ECOLOGY OF GROUND-DWELLING CARABID BEETLES (COLEOPTERA:
CARABIDAE) IN THE PERUVIAN ANDES
BY
SARAH A. MAVEETY
A Dissertation Submitted to the Graduate Faculty of
WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCES
in Partial Fulfillment of the Requirements
for the Degree of
DOCTOR OF PHILOSOPHY
Biology
December 2013
Winston-Salem, North Carolina
Approved By:
Robert A. Browne, Ph.D., Advisor
Terry L. Erwin, Ph.D., Chair
T. Michael Anderson, Ph.D.
William E. Conner, Ph.D.
Miles R. Silman, Ph.D.
ACKNOWLEDGMENTS
First, I would like to thank to my advisor, Dr. Robert Browne, who has played a pivotal role in my time at Wake Forest University, encouraging and supporting my research endeavors since my sophomore year as a biology undergraduate. I would also like to thank Biology Department committee members, Dr. Miles Silman, Dr. Bill Conner,
Dr. Michael Anderson. The dissertation research would not have taken place in Peru had it not been for Dr. Silman’s long standing research presence there, and I am grateful for his connection. Dr. Conner was my first professor in biology ten years ago, and he has given invaluable insight as the first reader of the dissertation. Dr. Anderson provided instrumental ecological perspective in both my academic career and dissertation. A special thanks to my outside committee member, Dr. Terry Erwin, Curator of Coleoptera at the Smithsonian National Museum of Natural History, and Neotropical carabid beetle expert. He has dedicated his time and expertise so that my specimens were identified correctly and I made all the appropriate connections to colleagues in both Peru and the
U.S.
The field portion of this project was supported by a Fulbright Grant to conduct research in Peru, and I thank the onsite staff of the Comisión de Fulbright in Lima, Peru. I am also grateful to colleagues at the Museo de Historia Natural Universidad Nacional
Mayor de San Marcos, Dr. Gerardo Lamas, Juan Grados, and Luis Figueroa, for help in obtaining permits for beetle collection and exportation. For assistance with field logistics
I’d like to thank: Asocación para la Conservación de la Cuenca Amazonica (ACCA);
Daniel Blanco at PeruVerde; ProNaturaleza; students and professors at Universidad
Nacional San Antonio del Abad Cusco and the Museo de Historia Natural, especially my
ii field assistants Jessica Ttito Quispe and Carla Chaparro Zamalloa; and Hubert Jaquehua
Callo, No lo hubiera logrado sin ti.
Finally, I want to thank former Browne lab graduate students Carmen Chavez and
Doug Bruce for sharing Appalachian ground beetle data, and to all the undergraduates who helped in data collection and helped me to meticulously measure individual body lengths. Thank you to my all friends at Wake Forest University, but especially to Rachel
Hillyer for her friendship and for help studying for preliminary exams, and to Katie Riley, for going through the ups and downs of graduate school as both a best friend and colleague. I thank my best friends from home, Jessica Young, Tracey Young, and Kasee
Metcalf for always being there for me. But above all I am most grateful for the constant loving support of my family who have always encouraged me to do my best.
iii TABLE OF CONTENTS
ACKNOWLEDGMENTS ...... ii
LIST OF TABLES ...... vii
LIST OF FIGURES ...... ix
ABSTRACT ...... xi
CHAPTER I
Introduction ...... 1
CHAPTER II
Carabidae diversity along an altitudinal gradient in a Peruvian cloud forest (Coleoptera)
Published in Zookeys (2011)
ABSTRACT ...... 18
INTRODUCTION ...... 19
METHODS ...... 22
RESULTS ...... 26
DISCUSSION ...... 29
LITERATURE CITED ...... 34
APPENDIX ...... 51
CHAPTER III
Carabid beetle diversity and community composition as related to altitude and seasonality in Andean forests
Accepted for publication in Studies on Neotropical Fauna and Environment
(December 2013)
iv ABSTRACT ...... 53
INTRODUCTION ...... 54
MATERIALS AND METHODS...... 57
RESULTS ...... 59
DISCUSSION ...... 61
REFERENCES ...... 67
CHAPTER IV
Effect of disturbance and inter-annual variation on carabid beetle assemblages in an Andean cloud forest
To be submitted to Journal of Tropical Ecology (December 2013)
ABSTRACT ...... 81
INTRODUCTION ...... 82
METHODS ...... 86
RESULTS ...... 91
DISCUSSION ...... 95
LITERATURE CITED ...... 101
APPENDIX ...... 126
CHAPTER V
Patterns of carabid beetle (Coleoptera: Carabidae) morphology along a Neotropical altitudinal gradient in the Peru
Submitted to Ecological Entomology (August 2013)
ABSTRACT ...... 129
INTRODUCTION ...... 131
MATERIAL AND METHODS ...... 135
v RESULTS ...... 140
DISCUSSION ...... 144
CONCLUSIONS ...... 150
REFERENCES ...... 152
CHAPTER VI
Carabid beetle assemblages (Coleoptera: Carabidae) on Andean and Appalachian altitudinal gradients
To be submitted to Environmental Entomology (December 2013)
ABSTRACT ...... 169
INTRODUCTION ...... 170
MATERIAL AND METHODS ...... 173
RESULTS ...... 177
DISCUSSION ...... 181
REFERENCES CITED ...... 187
CHAPTER VII
CONCLUSIONS AND FUTURE DIRECTIONS ...... 204
APPENDIX ...... 212
CURRICULUM VITAE ...... 261
vi LIST OF TABLES
Table II-1. Locality data for the five altitudinal sites ...... 41
Table II-2. List of all tribes, genera and morphospecies ...... 42
Table II-3. Site specificity by taxa ...... 43
Table III - 1. Comparison of total number of carabid beetle morphospecies between
seasons and altitudinal zones ...... 72
Table III - 2. Carabid beetle diversity and dominance indices by season and altitude ..... 75
Table IV - 1. Summary of individuals and species collected by altitudinal zone ...... 112
Table IV - 2. Description of altitudinal zones for the disturbed gradient ...... 113
Table IV - 3. Number of individuals and species and diversity and community metrics for
altitudinal zones along the disturbed and the old growth gradients ...... 114
Table IV - 4. Partitioned beta diversity by altitude ...... 115
Table IV - 5. Number of individuals and species and diversity and community metrics for
the different collection years ...... 116
Table IV - 6. Index of species temporal turnover by collection year ...... 117
Table V - 1. Description of wing state ...... 160
Table V - 2. Flight muscle correlation with altitude between macropterous and
brachypterous wing states ...... 161
Table V - 3. Apparent body length, flight muscle, and wing state of carabid beetles
between the disturbed and old growth gradients ...... 162
Table VI - 1. Species richness by altitudinal zone for Appalachian and Andes carabid
beetles ...... 194
Appendix Table A1. Summary of collection sites for Andean data set ...... 212
vii Appendix Table A2. Summary of collection sites for Appalachian data set ...... 213
Appendix Table A3. Adjustment coefficients per site for hand collections ...... 214
Appendix Table A4. Distribution of 55 most abundant morphospecies ...... 215
Appendix Table A5: Average body length of morphospecies ...... 218
viii LIST OF FIGURES
Figure II - 1. Map of collection sites ...... 45
Figure II - 2. Species accumulation curves for five diversity indices ...... 46
Figure II - 3. Number of species and altitude ...... 47
Figure II - 4. Percentage of rare species and altitude ...... 48
Figure II - 5. Species accumulation curves for each collection type ...... 49
Figure II - 6. Non-metric multidimensional scaling of altitude and collection method .... 50
Figure III - 1. Species accumulation curves for rainy and dry season collections ...... 77
Figure III - 2. Number of species as a function of (A) species accumulation, and (B)
altitude ...... 78
Figure III - 3. Ordination by non-metric multidimensional scaling ...... 79
Figure IV - 1. Map of study area ...... 119
Figure IV - 2. Species accumulation for the old growth and disturbed gradients ...... 120
Figure IV - 3. Rarified species richness by altitudinal zone and beta diversity for the old
growth and disturbed gradients ...... 121
Figure IV - 4. Non-metric multidimensional scaling comparing old growth and disturbed
gradients ...... 122
Figure IV - 5. Relative abundance plots for the disturbed and old growth gradients ..... 123
Figure IV - 6. Species accumulation for the different collection years ...... 124
Figure IV - 7. Non-metric multidimensional scaling for interannual comparisons ...... 125
Figure V - 1. Map of study area and location of collection sites ...... 164
Figure V - 2. Altitudinal trends in apparent body length ...... 165
Figure V - 3. Altitudinal trends in flight muscle length ...... 166
ix Figure V - 4. Altitudinal trends in per cent brachyptery...... 167
Figure VI - 1. Map of sampling sites ...... 197
Figure VI - 2. Species accumulation for Appalachian and Andean carabid beetles ...... 198
Figure VI - 3. Rarified species richness by altitude for Appalachian and Andes sites ... 199
Figure VI - 4. Non-metric multidimensional scaling for Appalachian and Andean carabid
beetle species assemblages ...... 200
Figure VI - 5. Relative abundance plots for Appalachian and Andean carabid beetle
assemblages ...... 201
Figure VI - 6. Mean body length of carabid beetles as a function of altitude...... 202
Figure VI - 7. Percent flightless carabid beetle species by altitude ...... 203
Appendix Plate A1. Macropterous wing condition (Notiobia E) ...... 225
Appendix Plate A2. Brachypterous wing condition (Galerita A) ...... 226
Appendix Plate A3. Brachypterous wing condition (Dercylus A) ...... 227
Appendix Plate A4. Micropterous wing condition (Dyscolus A) ...... 228
Figure A1. Illustrations of elytral markings on select carabid beetle species ...... 260
x ABSTRACT
Maveety, Sarah A.
ECOLOGY OF GROUND-DWELLING CARABID BEETLES (COLEOPTERA: CARABIDAE) IN THE PERUVIAN ANDES
Dissertation under the direction of
Dr. Robert A. Browne, Professor of Biology
Studies of diversity and species distributions are crucial in light of a predicted 4-
6°C warming by the end of the 21st century, especially in the tropics where many species may be especially sensitive to climate change. Little is known about patterns of insect diversity and richness in Andean montane forest habitats. The main goal of the present research was to investigate the ecology of carabid beetles at different altitudes in southeastern Peru (Coleoptera: Carabidae). Changes in species richness, species assemblages, and wing and body attributes were estimated at different altitude zones along both disturbed and undisturbed gradients.
My first objective was to estimate species richness patterns of carabid beetles on
Andean slopes. Preliminary collections employed both hand collections and pitfall traps, but I found that hand collections were more efficient; subsequent data collection was carried out by hand collections. Preliminary data collected on an anthropogenically disturbed gradient from 1400 m to 3450 m revealed a decline in raw species number with altitude. When species number was adjusted for sample size (rarefaction) this trend produced a middle altitude peak in species richness. A truncated portion of the disturbed
xi gradient (2000 m to 3450 m) was also compared to a parallel, old growth gradient, and no pattern was found with altitude for either gradient. However, overall species richness was lower for assemblages from the disturbed gradient. Species assemblages varied by altitude and by whether anthropogenic disturbance had occurred.
The second objective was to characterize changes in body length and dispersal ability with altitude. For both morphological attributes, altitudinal patterns were highly variable among tribes of carabid beetles, exhibiting positive, negative and no correlation with altitude. When carabid beetle taxa were combined, however, body length and incidence of flightlessness were both significantly negatively correlated with altitude.
Observation of morphological characters between the two gradients revealed that carabid beetles on an anthropogenically disturbed habitat were longer and had greater dispersal ability than those on an old growth gradient.
The third objective was to compare assemblages of carabid beetles in the Andes of Peru to a temperate counterpart in the southern Appalachian Mountains, USA. Species richness of carabid beetle assemblages was found to be approximately twice as high in the Andean assemblage. Both assemblages showed a middle altitude peak in species richness. Furthermore, species composition of carabid assemblages had no overlap at the species and genus level, but species composition in both the Andes and the Appalachians varied with altitude. Body length was greater and dispersal ability was reduced for
Appalachian as compared to Andean assemblages. Both regions exhibited similar patterns in body length in relation to altitude. However, while the proportion of flightless species was positively correlated with increasing altitude in the Andes, more than 90% of the species in the Appalachians were flightless at all elevations.
xii I suggest the altitude-species richness trend may be more conclusive when a more complete altitudinal gradient is sampled, i.e., extending sampling along the entire length of the gradient. Furthermore, employing multiple study transects will enhance statistical validity of the results and greatly increase our knowledge of how carabid beetle assemblages vary along tropical altitudinal gradients.
xiii CHAPTER I
INTRODUCTION
Altitudinal gradients
How organisms are distributed along altitudinal gradients in tropical and temperate montane forests has been a long-standing question (e.g., Humboldt and Bonpland 1807;
Whitaker 1956). Montane systems are an ideal setting to study species distributions because environmental factors often vary predictably with the altitudinal gradient
(Lessard et al. 2010). Increasing altitude is coupled with decreased temperature (lapse rate ca. 5.5°C km-1) and partial pressure of respiratory gases, and increased precipitation and wind velocity (Hodkinson 2005). These changes in the physical environment make altitudinal gradients an excellent natural laboratory (Malhi et al. 2010).
Studies of species distributions and biodiversity are especially crucial in light of a predicted 4-6° C warming by the end of the 21st century (Feeley and Silman 2010). The impact of impending climate change may be especially pronounced for tropical montane habitats. Projected warming trends are expected to shift current climate states both pole- ward and up mountains, potentially resulting in novel climates in tropical lowlands and the disappearance of extant high altitude climates, especially for the tropical Andes
(Williams et al. 2007). Evidence of shifting climate states has been observed in ice cap contraction (Bush et al. 2004, Thompson et al. 2006) and disappearance of small glaciers
(Young 2008). Upslope species range shifts are predicted pending increased warming
(Feeley and Silman 2010), and have been reported for some bird species in Costa Rica
(Pounds et al. 1999), anuran populations in Peru (Seimon et al. 2007), and geometrid
1 moths in Borneo (Chen et al. 2009). In a meta-analysis of various taxa, Chen et al. (2011) reported that distributions of organisms have recently shifted upslope at a median rate of
11 m decade-1.
As climate warms, altitudinal gradients may act as potential “arks” for biodiversity, offering the possibility of upslope migration for some species (Malhi et al.
2010). However, timberline migration is occurring at a slower pace than that required for most warming scenarios (Rehm and Feeley 2013). Even if species are capable of migrating, the upper limit of the forest might hinder retreat. High altitude specialists may be the most threatened because of potential loss of habitat (Laurance et al. 2011, Sheldon et al. 2011).
There is no universal pattern of species richness along an altitudinal gradient.
Two trends, however, are most pervasive in the literature: species richness declines monotonically with altitude, e.g., Neotropical tree species (Gentry 1988) and syntopic birds in Peru (Terborgh 1977), or there is a peak at the middle altitudes, e.g., small mammals in Costa Rica (McCain 2004) and Neotropical land birds (Rahbek 1997).
McCoy (1990) suggested that the monotonic decrease seen in diversity with increasing altitude can be explained by a reduction in habitat area, resource diversity, and primary productivity and the increasingly harsh abiotic environment. Another possible explanation of the decline in species richness relates to species ranges. Rapoport’s Rule predicts the reduction in species ranges with decreased latitudes accounts for increased diversity in the tropics (Stevens 1989), is often applied to explain species richness along altitudinal gradients (Stevens 1992, Rahbek 1997).
2 A peak in species diversity at intermediate altitudes has a long history in the literature (e.g., sweet samples of insects in Venzuela, Janzen et al. 1976, and netted bird species in Peru, Terborgh 1977). Recently, the middle altitude peak in species richness is most often attributed to a physical phenomenon known as the mid-domain effect (MDE).
As a null model, MDE hypothesizes that species ranges within a geometric boundary are more likely to overlap towards the middle of the gradient (Colwell and Lees 2000). Moret
(2009) suggests that a middle altitude hump in species richness can be attributed to the overlapping ranges of lower and upper limited species.
Sampling regime may influence the discrepancies observed for altitudinal species richness patterns. For example, a negative relationship between bird diversity and altitude transforms into a middle altitude hump when samples are standardized by collection technique (e.g., mist netted birds only; Terborgh 1977). Rahbek (1995) further showed that taking into account size of sampling area converts the linear trend to a middle altitude peak in richness. Nogués-Bravo et al. (2008) suggested that the relationship between species diversity and altitude depends on scale. When the entire gradient is sampled, a middle altitude peak in richness is evident, but as spatial scale decreases, the pattern becomes progressively monotonic.
Due to increased temperature and aridity associated with climate change and from forest degradation from anthropogenic disturbance, the montane forests of the Andes in southeastern Peru are among the most threatened forests on earth (Williams et al. 2007,
Sheldon et al. 2011). Understanding changes in biodiversity, due to direct causes such as land conversion and indirect causes such as climate change, requires baseline data; one of
3 the aims of the present research was to establish baseline data for carabid beetles in
Andean Peru.
Carabid beetles
With approximately 1.4 million species described, insects represent 80% of all life recorded on Earth (Erwin 1996). Within Insecta, beetles are the most speciose, comprising more than 25% of all described species on Earth (Erwin 1996), and carabid beetles are one of the most diverse beetle families (Erwin 1991), within the top five families.
Carabid beetles are a very ubiquitous taxon. They occur, or have occurred, almost everywhere on the planet except the deep ocean since the Triassic (Erwin 1996). Carabids are varied in morphology, way of life, behavior, and biotopes occupied (Niemelä et al.
2000) and play a role in the majority of ecosystem processes, such as predators, herbivores, folivores, detritivores, scavengers, frugivores, wood-eaters, grazers, etc.
(Erwin 1996). While the majority of carabid species are epigeic, or ground dwelling, many species are also adapted to waterside, canopy, or cave habitats, etc., especially in the tropics (Darlington 1943).
Carabid beetles are frequently employed as model organisms for ecological study because of high species diversity, relative ease of collection and subsequent taxonomic description, and they are known indicators of ecological and environmental change
(Erwin 1996, Niemelä et al. 2000). The majority of ground beetle studies are from boreal and temperate regions (Rainio and Niemelä 2003). Most work on Neotropical carabids has focused on the lowland Amazonian rainforests (in Peru, see Erwin 1991, or in
4 Ecuador, see Lucky et al. 2002), or the high alpine zone (Ecuador: Moret 2005, 2009).
Little is known about the fauna and ecology of carabid beetles in montane Andean forests.
Many of the facets that make carabid beetles ideal for study in temperate regions can become problematic in the tropics. For example, the high diversity of carabid beetles is both a boon and a burden for tropical research; while sampling yields both a high number of species and individuals necessary for adequate analysis, it causes problems for taxonomic classification (Niemelä 1996, see also Brehm et al. 2007). In addition, the ease of passive collection methods, e.g., pitfall traps, have added to the popularity of carabids as model organisms, although this type of method is not as successful for tropical carabid fauna. As a whole, tropical arthropods are difficult to sample (Brehm et al. 2007), as compared to the temperate counterparts, where techniques have been more tested through time.
Objectives
Patterns of insect diversity in Andean montane forest habitats are not well known (Brehm et al. 2003). The overall goal of the research presented here is to document carabid beetle diversity and ecology in altitudinal montane biotopes of the eastern Andean slopes in
Peru.
In Chapter II, I examine the qualitative diversity and community composition of carabid diversity in the cloud forests of southeastern Peru based on collections of carabid beetles in 2007 – 2008. I report change in raw species richness with altitude and incidence of rare and altitude restricted species. Both active and passive collection methods (i.e., hand collections and pitfall traps) are employed and diversity and
5 compositional differences are presented. The efficacy of hand collections versus pitfall traps in the tropics is compared.
In Chapter III, the same data from collections in 2007 to 2008 are used to address questions about spatial and temporal variation of carabid beetle assemblages along the altitudinal gradient. The primary focus is to obtain estimates of species diversity and community composition along this altitudinal gradient in montane Andean forests, with repeated sampling throughout an annual cycle (2007 to 2008), including both rainy and dry seasons. I test whether rarified species richness will decrease with elevation, coupled with a change in community composition, reflecting the increasingly harsh climate and restrictive abiotic environment seen as altitude increases. I also test whether seasonality will influence diversity since humidity is a limiting factor for carabid beetle diversity
(Lövei & Sunderland 1996) and seasonal variability has been reported in carabid beetle assemblages in lowland tropical rainforests (Lucky et al. 2002).
In Chapter IV, I compare carabid beetle diversity along two parallel altitudinal gradients in southeastern Peru: one characterized by anthropogenic disturbance and the other within an old growth forest. The impact of anthropogenic disturbance on species rich insect communities in the tropics is largely unknown (Brehm and Fiedler 2005), and the effects of habitat degradation are likely to both compound and confound the effects of climate change on species diversity and distribution (Larsen 2012). I analyze patterns of species richness, based on richness estimators, and diversity and community metrics, and examine the impact of anthropogenic disturbance on composition of carabid beetle assemblages. Inter-annual changes in richness and composition of carabid beetles
6 collected over three census intervals based on collections from 2008, 2010, and 2011 are examined.
In Chapter V, I present data for changes in two morphological characters, body length and wing condition, along the altitudinal gradient. The process of loss of flight in carabid beetles has been examined (Darlington 1936, Kavanaugh 1985) and flightlessness has been observed in high altitude carabid fauna (e.g., North America: Darlington 1943,
Caribbean: Darlington 1970, and Scandinavia: Nilsson et al. 1993). However, this is the first analysis of flightlessness in carabid beetles as related to change in altitude in Andean forests. Because of both abiotic constraints and increasing environmental homogeneity, I test whether there is a decrease in body length and flight capability with increasing altitude. In addition, differences in body length and dispersal ability along an old growth forest gradient and an anthropogenically disturbed gradient are also examined. Because of the relative instability of disturbed habitats, carabid beetles would likely be more vagile, i.e., need a higher degree of dispersal ability, to maintain populations.
In Chapter VI, carabid beetle diversity is compared between the tropical assemblage of the Andes in Peru and a temperate assemblage from the southern
Appalachians in the USA. Although temperate species richness is lower than in the tropical counterpart (e.g., Gentry 1988) the limited abiotic environment encountered with increasing altitude may still reveal similar patterns in altitudinal species distributions. In this chapter, I analyze the difference in rarified richness, community composition, body length and dispersal ability of carabid beetles between tropical and temperate regions.
In Chapter VII, I summarize the findings of my research, and discuss potential future directions. Appendices provide supplementary material that may be found useful in
7 reference to the collected data: A1) GPS and locality data for Andean collections; A2)
GPS and locality data for Appalachian collections; A3) matrix of search effort (hand collections) by altitudinal zone and collection year; A4) distribution of 55 most abundant species by altitude; and, A5) average body length of morphospecies by altitude. Images of select wing conditions for carabid beetles can be found in Plates 1-3. Finally, a preliminary diagnosis to morphospecies is presented, which has been edited with guidance from Dr. Terry L. Erwin, Coleoptera curator at the Smithsonian National
Museum of Natural History. This is included for the aid of future collections of
Carabidae in Neotropical montane forests.
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16 CHAPTER II
CARABIDAE DIVERSITY ALONG AN ALTITUDINAL GRADIENT IN A
PERUVIAN CLOUD FOREST (COLEOPTERA)
Published:
Maveety, S.A., Browne, R.A., & Erwin, T.L. 2011. Carabidae diversity along an
altitudinal gradient in a Peruvian cloud forest (Coleoptera). Zookeys. 147, 651-
666.
Stylistic variations are due to the requirements of the journal. Slight modifications were made after publication.
17 Abstract
Carabid beetles were sampled at five sites, ranging from 1400 m to 3400 m, along a 15 km transect in the cloud forest of Manu National Park, Perú. Seasonal collections during a one year period yielded 77 morphospecies, of which 60% are projected to be undescribed species. There was a significant negative correlation between species richness and altitude, with the number of carabid species declining at the rate of one species for each 100 m increase in altitude. The majority of species (70.1 %) were restricted to only one altitudinal site and no species was found at more than three of the five altitudinal sites. Only one genus, Pelmatellus (Tribe Harpalini), was found at all five sites. Active (hand) collections yielded approximately twice as many species per individuals collected than passive (pitfall trap) collections. This study is the first systematic sampling of carabid beetles along a high altitude gradient in Andean forests and supports the need to conserve the zone of extremely high biodiversity present on the eastern slopes of the Peruvian Andes.
Keywords: Ground beetles, tropical montane forests, Neotropics, pitfall traps, Andes
18 Introduction
Tropical forests may support up to 80 percent of the world’s biodiversity (Wilson 1992).
In tropical montane cloud forests, moisture from the lowland forest rises and cools, enshrouding the area in heavy mist for at least part of each day (Lawton et al. 2001).
With increasing altitude, temperature decreases, while condensation and precipitation increase, resulting in high humidity and relatively cool temperatures in montane cloud forests (Kricher 1997). Most high altitude tropical forests of the new world, including those found in the Andes, are dominated by cloud forests which support high levels of endemism and insularity (Schonberg et al. 2004). In the Andes Mountains of Perú, cloud forests generally exist at approximately 2000 to 3500 m (Kricher 1997) but can be locally variable, occurring as low as 1500 m in certain areas such as the K’osñipata Valley in southeastern Perú, the location of this study.
As with lowland rain forests, montane cloud forests are subject to numerous threats, including logging and land conversion to agriculture and pasturage (Kricher
1997; Schonberg et al. 2004); the destruction of nearby lowland tropical forest can also have an indirect and negative impact on montane cloud forests (Lawton et al. 2001). As climate change becomes more than just a prediction, cloud forests are expected to retreat with appropriate habitat shifting to higher, often anthropogenically disturbed altitudes, potentially affecting every organism within these highly fragile ecosystems (Nadkarni and Solano 2002; Pounds et al. 1999). Because of these expected transformations, research on cloud forest habitats can offer valuable insight on the effects of climate change.
19 Biological organisms are useful as indicators of local habitat change and as estimators of forest fluctuations due to fragmentation or climate change (e.g., Jennings and Tallamy 2006; Chen et al. 2009). Understanding changes in biodiversity, due to direct causes such as land conversion, and indirect causes such as climate change, requires a baseline inventory. In the cloud forests of southeastern Perú, only limited data are available on biodiversity, and are further restricted to only a few taxa, such as birds
(see Terborgh 1977), flowering plants (Gentry 1988), and a few insect groups, e.g., wasps
(Castillo-Cavero 2009), and ants (Azorsa-Salazar 2009). However, for one of the most diverse taxa, Coleoptera, baseline data are few for this critical habitat. Previously conducted tropical inventories have focused on lowland areas while data on montane areas is often lacking (Brehm et al. 2003; Schonberg et al. 2004). Species richness of many taxa is generally higher in the lower altitudes of a tropical altitudinal cline; e.g., trees (Kricher 1997), birds (Terborgh 1977), and insects (McCoy 1990; Escobar et al.
2005; Hanski and Niemela 1990). However, the number of endemic bird species in South
America is approximately twice as high for high altitude cloud forests than adjacent lowland rain forests (Stotz et al. 1996). Relatively little work has been done on the use of insects as biodiversity indicators in these tropical montane forests. Although a preliminary study of Carabidae community composition in the lowland Amazon Basin of
Perú was reported by Erwin (1991), no studies have been conducted on the biodiversity of
Carabidae on the highly diverse and imperiled tropical Andean slopes. Carabid beetles may be especially good biodiversity indicators because they can successfully signal environmental and ecological change (Niemelä et al. 2000, Desender et al. 1999) but they also vary widely in morphology, taxonomy, behavior and ecology (Erwin 1996).
20 Carabidae are also easily collected and their identification for analysis is relatively uncomplicated (Erwin 1996). Importantly, carabid beetle collections appear to be representative of the composition of arthropod fauna in general (Butterfield et al. 1995).
In many areas of the tropics, where biodiversity is especially high but poorly inventoried, ecological researchers often encounter what has been termed the “taxonomic impediment” (New 1984, Cardosa et. al 2011), which is characterized by a difficulty in identification of species due to a lack of systematic classification (Samways 1994). This
“taxonomic impediment” can be overcome by continuing baseline studies in an attempt to catalog all diversity for future studies and synthesizing the objectives of taxonomy (e.g., inventory) and of ecological studies (e.g., uncovering patterns). However, as an intermediate step, the usual approach for ecological analysis is to classify new species as morphospecies. Given the lack of taxonomic keys for tropical, and especially Neotropical montane carabids, the morphospecies approach was utilized for the majority of the taxonomic work for this study. Since the effects of global climate change are expected to be the most severe for tropical insect communities, compared to their temperate counterparts, (Deutsch et al. 2008), inventory studies are especially needed in these areas.
In the present study, carabid beetles were collected from sites located on an altitudinal cline in the Andes Mountains in order to estimate absolute species diversity and extrapolated species richness. Incidence of rare and altitudinally restricted species is evaluated. Both active and passive collection methods were employed and the efficacy of these methods is compared.
21 Methods
Field study
Carabid beetles were collected at sites adjacent to the Cusco-Pilcopata highway in the
Cultural Zone of Manu National Park, Department of Cusco, in southeastern Perú. Five sampling sites were established at approximately 500 m altitudinal intervals: Acjanaco
Control Point (3400 m); Wayqecha Biological Station (2900 m); Pillahuata Research
Station (2500 m); Rocotal (2000 m); and San Pedro (1400 m). The transect altitude decreases 1900 total meters over 15 km distance. Table 1 presents the GPS and altitude locality data for all sites. Geographical locations of the sites are depicted in Figure 1.
At each site, carabid beetles were collected passively (pitfall traps) and actively
(hand searches). Pitfall traps consisted of 1 liter plastic cups, the mouth inserted flush with ground level, with a plastic roof anchored by nails over the opening to prevent rain water from entering. Each trap was filled with salt water as a preservative and a small amount of soap to minimize surface tension. In order to account for possible microsite variation, two clusters of traps were placed at least 10 meters apart, with six traps per cluster for a total of 12 traps per site. Collections were conducted monthly from
September 2007 to July 2008 by S.A. Maveety and Peruvian assistants. Active collections were made by sifting through leaf litter along the forest floor and examining above ground vegetation to approximately 1.5 m in height. Hand collections were carried out at night due to the generally nocturnal behavior of carabid beetles and included an additional collection during December 2008. All beetles were preserved in 95% ethanol.
In order to provide an estimate of search effort, the number of collectors and the time spent searching was recorded for each site (see Table 1 of Appendix).
22 Since there were no previous collections in this area, a specific key to high altitude Neotropical carabid beetles and a list of species to this area were not available.
Specimens were therefore identified to genus using a Neotropical Carabidae key
(Reichardt 1977), a carabid beetle key to Pakitza, Manu N.P., Perú (Erwin 1991), and a key to tribes and genera of the Carabidae of Costa Rica (Erwin et al. 2004), and were subsequently identified to morphospecies level, with classification based on external morphology (not including genitalia). Identifications were made to morphospecies level by S. A. Maveety with an original estimated 3% error rate, which was subsequently lowered via identifications at the Smithsonian Institution National Museum of Natural
History by T. L. Erwin.
Data analysis
Species accumulation curves
Species accumulation curves plot the number of species against the cumulative number of individuals in samples and thus adjust species number for total sampling effort. As more individuals are collected only the rarest species are thought to be excluded from the collection; therefore the plotted line approaches a horizontal asymptote, i.e., the total number of species that occur in a sample. Smoothed species accumulation curves were constructed using EstimateS 7.52 (Colwell 2005). Various non-parametric estimators were used to examine species richness. Mao Tau estimates the number of species expected based on the sampled assemblage; A.C.E. (Abundance-based Coverage
Estimator) a coverage estimator, is based on a calculation of the species with abundances between one and 10 individuals because the most abundant species do not reveal much information about the assemblage; Chao 1 is an estimator that extrapolates the true
23 number of species in an assemblage based on number of singletons and doubletons in the sample; Jack, a first-order Jackknife estimator, is calculated based on the number of species that occur in only a single sample and attempts to reduce the underestimation of true S; and finally Bootstrap, a bootstrap estimator that draws randomly with replace from the data sample (for detailed descriptions of the richness estimators see Colwell and
Coddington 1994, Magurran 2004, or Colwell 2005). The following rarity estimates were also utilized from Colwell (2005): Singletons, the number of species with only one individual in total sample accumulated; Doubletons, number of species with only two individuals in total sample accumulated.
Rarity
The number of rare species was estimated using both a taxonomic and an ecological index. The taxonomic index accounts for rare species as singletons (when a species is represented by one specimen) and doubletons, etc., up to n = 5. Such an index is more often used in studies of diversity from a taxonomic perspective (e.g., Coddington et al.
1991). Conversely the ecological index accounts for species rarity as a percentage of the total sample (e.g., Arscott et al. 2006). Rare species in this study are defined as ≤ 1% of the total number of individual collected (i.e., n ≤ 19, based on a total of n = 1924 individuals), very rare species are represented by < 0.1% of the entire population (i.e., n ≤
2). Singletons are defined as n = 1 and doubletons as n = 2.
Ordination
Nonmetric Multidimensional Scaling (NMDS) in R 2.8.1
24 places similar data points close in the ordination space. For all NMDS analyses Bray-
Curtis similarity indices were used (Gotelli and Ellison 2013).
25 Results
A total of 1,924 carabid beetle specimens were collected, represented by 13 tribes, 22 genera, and 77 morphospecies (Table 1 and 2). The tribes with the most species are
Harpalini (represented by 27 morphospecies), Platynini (13 morphospecies) and
Bembidiini (13 morphospecies). These three tribes also contain the largest number of individuals collected: Harpalini (n = 1054), Platynini (n = 528), and Bembidiini (n = 118).
Among the five sites the greatest number of individuals collected occurred at 2900 m (n =
806), with the least number of individuals at 3400 m (n = 162).
Figure 2 shows the species accumulation curves when all collection sites are combined (n = 1924). The Mao Tau accumulation curve approaches but does not fully reach asymptote. Visual extrapolation of the curve suggests that an asymptote could occur at approximately 3000 collected individuals, with a total of 90 species. The Mao
Tau estimator is numerically lower than the four remaining richness estimators, as it only estimates S based on the observed assemblage (Gotelli and Ellison 2013). The other four diversity indices, A.C.E., Chao 1, Jack 1, and Bootstrap support the accumulating Mau
Tau species estimate (Figure 2), although at higher values for species richness. These diversity indices suggest that species number did not reach asymptote for the 2000 individuals collected. Figure 2 also shows the species accumulation curve (when all sites are combined) for rarity categories more commonly utilized by taxonomists (singletons and doubletons). Although the number of doubletons appears to asymptote at 1000 individuals the slope for singletons is positive up to the total number of individuals collected (1924).
26 As depicted in Figure 3, the total number of species collected varied significantly with altitude (χ2 = 14.46, P < 0.01), with the highest species richness (S = 28) found at both 2000 m and 1400 m. There is a significant negative correlation between S and altitude (r = 0.91, P < 0.05). Regression analysis (y = –0.010x + 46.7, Freg = 13.7, P <
0.05) indicates that the number of carabid species declines at the rate of 1.0% of the species diversity for each 100 m increase in altitude. Species numbers differed significantly (via χ2 tests based on magnitude array) among altitudes as follows: 1400 m =
2000 m ≠ 2500 m = 2900 m ≠ 3400 m. Number of genera and tribes represented in samples are also negatively correlated with altitude (r = 0.94, P <0.05; r = 0.91, P <0.05, respectively).
There was a high level of site specificity for species, genera and orders (Table 3).
The majority of species (70.1 %; 54/77) were collected at only one altitudinal site. Only
6.5% (5/77) of the species were found at three altitudinal sites and no species was found at more than three sites. At higher levels of taxonomic organization, similar trends, though less pronounced, occurred, with 45.5 % (10/22) of genera and 38% (5/13) of tribes limited to one altitude site. One Tribe (Harpalini) and only one genus within
(Pelmatellus) were found at all five sites.
Rarity was estimated from both taxonomic and ecological perspectives (Figure 4; see Materials and Methods for how rarity is estimated). Rare species constitute 29% of the carabid beetle community at the highest altitude, 3400 m, and > 50% at both the two lowest altitudes. At 1400 m, 71% species are rare using the taxonomic index and 85.7% are rare by the ecological index. There are significant negative correlations with altitude for both rarity indices (rtax = 0.951, reco = 0.953, P < 0.05).
27 Since collections included both active (hand) and passive (pitfall trap) methods, comparisons can be made between the two techniques. Active collections yielded a greater number of species per individuals collected than passive collections (Figure 5).
Since more than three times the number of individuals was collected actively than obtained via passive collections, the number of species obtained would be expected to be higher for the former. The number of species actively collected is significantly higher than for comparable size samples collected by passive techniques, i.e., for species richness rarified at 400 individuals sampled, hand collecting detected more than twice as many species (rarified richness was 17 for passive collections and 37 for hand collections,
P < 0.0001). When data are ordinated by non-metric multidimensional scaling (NMDS)
(Figure 6) the active and passive collection technique data points are not close together in space, suggesting that there is a compositional difference between carabid taxa collected actively or passively, especially at lower altitudes; however, data points are more clearly arranged by descending altitude on the x-axis.
28 Discussion
This study was the first inventory of carabid beetles for a high altitude gradient in the
Andean cloud forests. For approximately one year of collections, 77 morphospecies were collected. When more formal taxonomic analysis and a description of specimens are complete, approximately 60% of the species are expected to be previously undescribed
(TLE). Further sampling will likely result in even more unknown species. Biodiversity inventories of altitudinal gradients are particularly relevant since they can serve as studies of climate change. For example, Chen et al. (2009) repeated a taxonomic inventory of
Geometridae (Lepidoptera) in montane habitat in Borneo that had also been surveyed 40 years earlier. They found that average ranges of geometrid moths (102 species) had shifted upward by 67 m in altitude over the 40 year interval. Andean dung beetle ranges have recently increased 72 m in the past 10 years (Larsen 2010). These increases could be due to various factors, but were most likely the result of a shift in the altitudinal zone due to a changing climate.
Species accumulation curves allow for direct comparison of S at the alpha level, thus avoiding some of the pitfalls with other diversity indicators, such as Shannon and
Simpson indices (Veech and Crist 2010). The curves in the present analysis followed expected trends for tropical insects; when all samples are combined there is no evidence of asymptotic shape in the curve(s) indicating that the carabid beetle fauna has not been fully sampled with regard to the addition of new species. A continuously increasing species accumulation curve is expected for tropical insects (Escobar et al. 2005) because of the highly speciose nature of insects and the highly diverse nature of tropical regions.
29 As altitude increased, species diversity of carabid beetles decreased significantly.
Tree diversity along the same altitudinal transect that was used in this study is constant from the Amazonian lowlands (approximately 500 m) to 1500 m, then decreases from
1500 m to 3400 m (Gentry 1988; M. Silman pers comm.). Bird diversity parallels this change in vegetation diversity for altitudinal gradients in Perú (K’osñipata Valley,
Jankowski et al. 2013; Cordillera Vilcabamba, Terborgh 1977). Carabid beetle diversity may parallel the change in vegetation diversity on an altitudinal gradient either directly
(e.g., herbivorous species) or indirectly (e.g., predaceous species). Species number also decreases with increasing altitude for dung beetles in tropical Borneo (Hanski and
Niemelä 1990) and flying insects in Panama (Wolda 1987). An altitudinal study on temperate carabid fauna in Japan also reported a gradual decrease in species number along a gradient increasing in altitude (Hosoda 1999).
In addition to a significant change in species number with altitude, there is high degree of altitudinal site specificity, suggesting preferences for specific altitudes for the majority of carabid beetle species. Most species are confined to a single altitudinal site.
The physical extremes and abrupt changes in abiotic conditions, such as a decrease in temperature and partial pressure of respiratory gases as well as an increase in precipitation (Hodkinson 2005), may restrict carabid beetle communities to narrower altitudinal ranges. However, Stevens (1992) extended Rapoport’s rule to altitudinal gradients, which suggests that the breadth of altitudinal ranges of species tends to increase with altitude. Increasing altitude usually results in a decrease in resource diversity, reduced habitat area, increase in unfavorable environment, and decrease in primary productivity (McCoy 1990), which may lead to broader species ranges. Biotic
30 changes may also play a role. For example, the highest site, Acjanaco, at 3400 m, is near tree line, and the forest (elfin forest) possesses trees that are shorter in stature than those in lower altitudes; carabid beetles at 3400 m may be adapted to these conditions. Because of the absence and reduced size of trees, as well as abiotic factors, a smaller proportion of winged species would be expected at the highest altitudes (Darlington 1943; Poulsen
1996). A related study (Chapter V) indicates that the percent of flightless species is negatively correlated with altitude. Other studies in the Andes region have found that geographically restricted scarab beetles were negatively correlated with altitude (Escobar et al. 2005).
The dominant tribe collected in the study area was Harpalini; this group is composed of species that are mostly fully winged, and many Neotropical species are seed eaters (Arndt et al. 1996). Harpalini is one of the more speciose tribes of Carabidae
(Cieglar 2000) and is represented in this collection by 2 genera, Pelmatellus and Notiobia.
In the Neotropics, Pelmatellus is a high altitude genus with a body length of < 11 mm while Notiobia’s body length is generally > 10 mm and inhabits lower altitudes (Goulet
1974; Arndt 1998). The data from this study supports this observation since Notiobia was only found at the 1400 m and 2000 m sites, while Pelmatellus occurred along the entire gradient. Although sampling did not extend to altitude < 1400 m, we would speculate that
1400 m would be the lower limit for Pelmatellus while Notiobia and other genera would comprise the lowland Harpaline fauna at < 1400 m.
This was one of the first studies in a tropical montane environment to use both active and passive collecting techniques, which several studies suggest is necessary for complete inventories (e.g., Longino et al. 2002, Coddington et al. 1991). Species richness
31 estimates obtained from species accumulation curves suggested that active collecting produced almost twice as many species as did passive collecting for the same number of individuals sampled. Many carabid beetle studies, more often from temperate climates, employ pitfall trapping as it is a relatively simple and passive means of collection
(Günther and Assman 2004; Liu et al. 2007). However, there are potential drawbacks associated with this technique. Pitfall traps may not accurately represent the true density of carabid fauna because they inherently measure species activity to represent species abundance (Greenslade 1964; Gutiérrez and Menéndez 1997; Lenski 1982). Nevertheless,
Günther and Assmann (2004) have found that at least for two carabid beetle species there is a possible strong relationship between relative densities measured by pitfall traps and absolute density. Liu et al. (2007) disagrees, supporting that pitfall traps do not give a complete inventory of total carabid fauna present. This was clearly the case for carabid beetles collected in the present study, where more species were obtained from active collection than by passive pitfall traps (for the same sample size). Passive collections may only sample a small portion of the carabid beetle fauna in the tropics where carabid beetles fill a variety of niches including predators, herbivores, folivores, detritivores, scavengers, frugivores, wood-eaters, and grazers (Erwin 1979). Species that are not often caught by pitfall traps are relatively easy to collect by active hand collection, as was the case in this study. The “duff” composition of the soils in the Andean cloud forests where there is a high level of non-decomposed organic material and numerous interstitial spaces among the material, which may allow carabids to travel below the nominal “soil” surface, may limit the effectiveness of pitfall trapping in this region.
32 Acknowledgements
We thank the Peruvian Ministry of Agriculture, INRENA, and SERNANP for collection and export permits; the Museo de Historia Natural de la Universidad Nacional Mayor de
San Marcos, especially Dr. Gerardo Lamas for permit coordination; and Amazon
Conservation Association (ACCA). Further, we thank the Fulbright Program, Wake
Forest University and the National Museum of Natural History at the Smithsonian for support.
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40 Table II - 1. Locality data for the five altitudinal sites.
Altitude Altitude Latitude Longitude No. No. No. (m) Band (S) (W) Individuals Genera Species AJANACO 3470 3400 13°11.79' 71°37.22’ 162 3 7
WAYQECHA – – – Trap A 2791 2900 13°10.99’ 71°35.07’ 806 6 21 Trap B 2947 13°11.55’ 71°35.28’ PILLAHUATA – – – Trap A 2436 2500 13°09.69’ 71°35.49’ 381 7 21 Trap B 2425 13°09.69’ 71°35.47’ ROCOTAL – – – Trap A 2084 2000 13°06.80’ 71°34.25’ 227 13 28 Trap B 2082 13°06.68’ 71°35.00’ SAN PEDRO – – – Trap A 1432 1400 13°03.37’ 71°32.83’ 348 12 28 Trap B 1427 13°03.37’ 71°32.81’
41 Table II - 2. List of tribes, genera and morphospecies of Carabidae collected.
Tribe Morphospecies No. Tribe Morphospecies No. Bembidiini Bembidion A 5 Pelmatellus H 281 Bembidion B 1 Pelmatellus I 8 Bembidion C 12 Pelmatellus J 113 Bembidion D 3 Pelmatellus K 15 Bembidion E 25 Pelmatellus L 2 Bembidion F 10 Trichopselaphus A 9 Bembidion G 1 Trichopselaphus B 1 Bembidion H 8 Lachnophorini Anchonoderus A 12 Bembidion I 10 Psesdophoriticus A 18 Bembidion J 5 Pseudophoriticus B 2 Bembidion K 6 Lebiini Calleida A 3 Bembidion L 25 Calleida B 1 Bembidion M 7 Lebia A 1 Cicindelinae Pseudoxycheila 5 Lebia B 1 lateguttata peruviana Oodini Dercylus A 1 Galeritiini Galerita A 29 Ozaeniini Pachyteles A 3 Galerita B 3 Pachyteles B 2 Galerita C 1 Pachyteles C 1 Galerita D 2 Perigonini Diploharpus A 1 Harpalini Goniocellus A 1 Platynini Dyscolus A 365 Notiobia A 2 Dyscolus B 29 Notiobia B 3 Dyscolus C 22 Notiobia C 18 Dyscolus D 6 Notiobia D 3 Dyscolus E 1 Notiobia E 7 Dyscolus G 4 Notiobia F 15 Dyscolus H 1 Notiobia G 12 Dyscolus I 28 Notiobia H 2 Dyscolus J 3 Notiobia I 263 Dyscolus L 1 Notiobia J 1 Dyscolus K 1 Notiobia K 2 Dyscolus M 1 Notiobia L 3 Glyptolenus A 66 Pelmatellus A 1 Pterosticini Loxandrus A 1 Pelmatellus B 9 Loxandrus B 2 Pelmatellus C 276 Pseudobarys A 1 Pelmatellus D 3 Trichonilla A 1 Pelmatellus E 1 Scaritini Ardistomus A 3 Pelmatellus F 2 Trechini Trechischibus A 124 Paratrechus Pelmatellus G 1 sensulatt 6
42 Table II - 3: Site specificity by taxa (see text for additional descriptions).
Number of Sites occupied 1 2 3 4 5 Species 54 18 5 0 0 Genera 10 7 1 2 1 Tribes 5 3 2 2 1
43 Figure Headings
Figure II - 1: Map of collection sites.
Figure II - 2: Species accumulation curves for five diversity indices when all altitudes and collection types (active or passive) are combined (n = 1924).
Figure II - 3: Number of species and altitude when all altitudes and collection types
(active or passive) are combined (n = 1924).
Figure II - 4: Percentage of rare species and altitude. Black bars represent the taxonomic rarity index and gray bars represent the ecological rarity index (see text for definitions of rarity).
Figure II - 5: Species accumulation curves for each collection type (active and passive) when all altitudes are combined (n = 1924). Brackets represent 95% confidence intervals.
Figure II - 6: Non-Metric Multidimensional Scaling (NMDS) using the Bray Curtis
Similarity Index of altitude and collection method (triangle: active, and circle: passive).
Values for each altitude are grouped by ovals.
44
Figure II ‒ 1
45
Figure II ‒ 2
46
Figure II ‒ 3
47
Figure II ‒ 4
48
Figure II ‒ 5
49
Figure II ‒ 6
50 Appendix
51 CHAPTER III
CARABID BEETLE DIVERSITY AND COMMUNITY COMPOSITION AS
RELATED TO ALTITUDE AND SEASONALITY IN ANDEAN FORESTS
The following manuscript has been accepted for publication in Studies on Neotropical
Fauna and Environment (12/2013). Stylistic variations are due to the requirements of the journal.
52 Abstract
Carabid beetle (Coleoptera: Carabidae) diversity and community composition was investigated along an altitudinal gradient from 1400 m to 3400 m in southeastern Peru, utilizing recently published data of the first systematic inventory of carabid beetles in the region. The study transect is located in one of the highest biological diversity regions in the world. Active and passive collection techniques were used to examine temporal (rainy and dry seasons) and spatial (altitude) structure of adult carabid beetle assemblages. After adjusting for collection effort, species richness, as estimated by Mao Tau richness, peaked at 2000 m, some 600 meters above the lowest sampled altitude in this study.
Similarity between species assemblages from different altitudinal sites was ≤ 52%.
Species richness was approximately 10% higher in the rainy season than the dry season, with 64% of species occurring in both seasons. Despite the importance of multi-seasonal survey sampling for Neotropical habitats, most surveys to date have been limited to the dry season. Studies of organisms that can serve as indicators of habitat shift along altitudinal gradients become increasingly relevant with predicted global climate change.
Keywords: altitudinal gradient; Carabidae; mid-domain effect; puna; southeastern Peru; tropical rainforest
53 Introduction
Species diversity and community assemblages are often examined on naturally occurring environmental gradients such as altitudinal transects. Distribution of organisms along altitudinal gradients in tropical forests has been a long-standing question (e.g., Humboldt and Bonpland 1807). Montane systems are an ideal setting to study species distributions because environmental factors often vary predictably with the altitudinal gradient
(Lessard et al. 2010). Distinct communities of insects are found along an altitudinal gradient because, as ectotherms, insects are especially sensitive to temperature change
(Deutsch et al. 2008). Altitudinal patterns of diversity have been well studied in insects groups such as Lepidoptera (Brehm et al. 2003, Chen et al. 2009) and Coleoptera, including families Scarabaeidae (Hanski & Niemelä 1990, Escobar et al. 2005) and
Carabidae (Darlington 1943, Hosoda 1999, Moret 2009). According to projected climate change models, many tropical montane ecosystems are likely to disappear as lowland habitats advance upslope (Williams et al. 2007). With recent estimates for terrestrial taxa suggesting that species distributions may increase in altitude at a rate of 11 m per decade
(Chen et al. 2011) it is important to begin documentation of current species distribution and richness patterns as a point of reference for future studies.
Maveety et al. (2011) described the diversity of carabid beetles (Coleoptera:
Carabidae) in the cloud forests of southeastern Peru (from approximately1500 m to 3400 m) over a one year period. Their results reported the first systematic collection of carabid beetles on an altitudinal gradient in the Neotropics. Collections included both active
(hand searches) and passive (pitfall trap) collections and reported that active hand searches are the preferred method for carabid beetle collections in the tropics. Active
54 (hand) collections yielded almost four times as many individuals as passive pitfall traps, and sampled approximately twice as many species; most species found in pitfall traps were also found in hand collections and the two techniques collected similar assemblages.
Multiple collection techniques are often employed for total biodiversity surveys (e.g., see
Erwin 1996), but hand collections have proved more efficient for ground surface collections of carabid beetles in the Neotropics (Maveety et al. 2011).
This study utilizes the same data set of Maveety et al. (2011), but here examines species diversity and community structure through space (altitude) and time (seasonality).
Various trends have been observed for diversity as it relates to altitude. Species richness declines monotonically with altitude, e.g., in Neotropical tree species (Gentry 1988), syntopic birds in Peru (Terborgh 1977), and raw species number of carabid beetles in
Peru (Maveety et al. 2011), or there is a peak at the middle altitudes, e.g., small mammals in Costa Rica (McCain 2004) and Neotropical land birds (Rahbek 1997). Lack of correlation between species richness and altitude has also been reported, but more often for organisms that operate on a more fine grain scale, e.g., fungal wood decomposers
(Meier et al. 2010) and microorganisms that follow pH more than climatic variables
(Fierer et al. 2011). One suggestion for the discrepancies among trends is that altitudinal gradients span many biotypes and that the unique species communities occurring within biotypes are likely then to influence diversity patterns (Rahbek 1997). Accordingly, we restricted the present study to montane ecosystems rather than sampling a more complete altitudinal gradient that would include the Amazonian lowlands and adjacent lower
Andean slopes.
Carabid beetle communities have been the focus of numerous ecological studies,
55 mostly from temperate forests (Hosoda 1999, Eyre et al. 2005). In any assessment of biodiversity it is important to accurately sample and estimate total species richness of the focal taxon within a defined area (Coddington et al. 1991). However, sampling for most carabid beetle studies has been restricted to short time periods with incomplete seasonal sampling (Lövei & Sunderland 1996). In tropical forests, systematic carabid beetle sampling has primarily been at lower altitudes (Erwin 1991, Lucky et al. 2002) with most studies lasting less than a few months, or random months across several years. The present study expands on the first survey of carabid beetles conducted in a tropical montane forest throughout an annual cycle and at multiple altitude zones.
Our primary focus was to look for assembly patterns for these beetles by estimating species diversity and community composition along an altitudinal gradient in montane Andean forests, with repeated sampling in both the rainy and dry seasons. Based on the increasingly harsh climate and increasingly simple biotic and abiotic environment as altitude increases, we predicted that carabid beetle species diversity will decrease with elevation, coupled with a change in carabid beetle species assemblages, due to turnover of species with different life history strategies with increasing altitude. Since precipitation and humidity decrease in the dry season (Rapp & Silman 2012), and low humidity has often been shown to be a limiting factor for carabid beetle diversity (Lövei & Sunderland
1996), we also predicted that seasonality would impact diversity.
56 Materials and Methods
Collections of Carabidae
Carabid beetles were collected in K’osñipata Valley, within the Cultural Zone of Manu
National Park, Department of Cusco, in southeastern Peru. Sampling sites and collection methods reported by Maveety et al. (2011) are corrected here due to new information: approximately500 m intervals from 1400 m (not 1500m) to 3400 m, using both active
(hand searches) and passive (pitfall trap) collection techniques. It is important to note that these collection techniques primarily sampled adult epigeic carabid beetle assemblages.
Pitfall traps were collected, with the contents of each cup drained and passed through a fine mesh strainer, approximately every 30 days, from September 2007 to July
2008. Active hand searches were performed at night, and on the same dates as the trap collections. Collections spanned both seasons, rainy and dry. In the K’osñipata Valley, rainy months occur from November to April, with dry months from May to October; however, precipitation is greater than evapotranspiration for all months, and dry season months receive less rainfall (Rapp & Silman 2012).
Identifications were made to the level of morphospecies as presented in Maveety et al. (2011).We realize this is a simplified, imperfect approach. However, we believe that morphospecies classification represents a reasonable trade-off between absolute taxonomic accuracy (which may take many years to achieve) and the generation of comparative estimates of species diversity for carabid assemblages for different elevations and for wet and dry seasons. It is important to note that initial identifications have been revisited and revised since the publication of Maveety et al. (2011), e.g., genera Trechischibus and Paratrechus had been misidentified and are now corrected,
57 with the number of individuals for each revised.
Species accumulation curves
Smoothed species accumulation curves were constructed with 500 randomizations using the Mao Tau richness estimator, which estimates the number of species expected based on the total sampled assemblage (EstimateS 7.52, Colwell 2013). Species accumulation curves were used to interpolate, or rarify, species numbers by sampling effort (i.e., number of individuals). Rarified richness values are presented as means ± standard deviation, and the difference in means of rarified richness for seasonal and altitudinal analysis was compared using p-values calculated in R 2.13.1
Diversity and community indices
Fisher’s alpha, non-parametric diversity indices, Shannon-Wiener and Shannon’s evenness, and the Berger-Parker index (dominance) were calculated to further elucidate diversity patterns for both seasonal and altitudinal diversity. Species turnover between seasons and by altitude was calculated by Sørensen’s dissimilarity index (beta diversity).
See Magurran (2004) for more detailed descriptions of these indices.
Ordination
Species composition by altitude and by season was analyzed via Non-metric
Multidimensional Scaling (NMDS), using PC-ORD Version 6
NMDS was calculated based on Sørensen’s index, using 500 runs with real data and 100 iterations; three dimensions were analyzed and the two dimensions with greatest r2 values are reported in the results.
58 Results
Species diversity
A total of 1,958 carabid beetles representing 72 morphospecies were collected. Although the majority (62%) of individuals were collected during the dry season (Table 1, Table 2), the rarified number of species (Sr) was significantly higher in the rainy season (62 ± 5.6) than the dry season (40 ± 3.7) (P = 0.0004, Figure 1). The higher values for diversity indices (i.e., Shannon-Wiener, Shannon’s evenness, and Fisher’s alpha) and dominance also occurred during the rainy season (Table 2).
Species accumulation curves for the five altitudinal sites are presented in Figure
2A. No species accumulation curve reached an asymptote, although at 2900 m and 3400 m a relatively small increase in sample size might result in asymptote. In contrast, the slopes of the lower altitude curves remain nearly constant, even as sample size increases.
Figure 2B depicts Sr (adjusted by the Mao Tau estimator and derived from the species accumulation curves) for each altitude. Sr varied significantly among all sites (G = 12.9,
P < 0.05), and peaked at 2000 m [2000 m ≠ 1400 m (P = 0.0498) and 2000 m ≠ 2500 m
(P = 0.0024)], but there was no difference in Sr for sites ≥ 2500 m. There was no significant linear or curvilinear correlation between Sr and altitude.
The highest values for Shannon-Wiener diversity, Shannon’s evenness, and
Fisher’s alpha occurred at 2000 m (Table 2), but dominance was lowest at 2000 m.
Fisher’s alpha is one of the more useful indicators of community diversity because of its independence of sample size, as evidenced by lack of correlation between the number of individuals and Fisher’s alpha value (r = 0.0096, P = 0.875). Furthermore, as indicated in
Table 2, 2500 m and 2900 m altitudinal zones were the most compositionally similar
59 (Sørensen’s dissimilarity index = 48%), with the greatest species turnover at the next lower altitudinal zone, between 2000 m and 2500 m (Sørensen’s dissimilarity index =
80%).
Community composition
Non-metric Multidimensional Scaling (NMDS) indicates that altitude has a pronounced effect on species composition (Figure 3). Since the data points of the different seasons did not cluster in any clear pattern there was no apparent seasonal effect. This is reinforced by the low beta diversity, 36% dissimilar assemblages (Table 2), the relatively low level of species overlap between seasons, with 17% of morphospecies unique to the dry and 28% unique to the rainy season. Axes 2 (x-axis) and 3 (y-axis) explained the greatest amount of variability (r2 = 0.144 and 0.131, respectively), with Axis 2 likely including an altitudinal effect since the points are arranged by descending altitude. The greatest morphospecies variability within an altitudinal zone occurred at 1400, which also had the highest proportion of unique species (32%). The 2000 m zone also had a relatively high proportion (21%) of unique species. In contrast, the upper three altitudinal zones each had less than 4% unique species. The lower two altitudinal zones included two tribes, Galeritini and Lachnophorini, which were not found at or above 2500 m.
Additionally, Bembidiini and Trechini, both tribes typical of high altitude environments, were not found below 2000 m (with Trechini only occurring at 2500 m and 3000 m zones).
60 Discussion
Seasonality
Seasonality is an important component of most biodiversity assessments. If the goal of a biodiversity study is a complete inventory of a specific higher taxon, a researcher should not only decide where (e.g., altitudinal gradient, physical location) and how (e.g., collection methods) to optimize the number of species sampled, but also when (e.g., time of year) collections should take place. Within the montane forests of the Peruvian Andes, we found a significantly higher number of species in the rainy season than during the dry season. Similar results were observed for insect species in the tropical lowlands of Costa
Rica and Caribbean (Janzen 1973) and for Coleoptera in the Canal Zone of Panama
(Erwin & Scott 1981). The increase in species number for our study could be related to compositional turnover, because communities were no more than 64% similar between seasons. Given the results of our study, we recommend that biodiversity studies include collections made during the rainy and dry seasons, with collections conducted periodically throughout each season.
The effects of inter-annual variation on carabid species diversity and community composition in the tropics are virtually unknown, and future studies will be needed to assess inter-annual variability. Erwin et al. (2005) found that three years of fogging (nine total sampling events) produce an asymptotic accumulation curve for carabid beetles in the lowland rainforest canopies. Because the collection methods of the present study, i.e., pitfall traps and hand collections, yield lower abundances, we suggest that at least five years would be needed to compare inter-annual patterns with confidence. Erwin et al. (in press) provide data from trans-seasonal and trans-annual canopy samples in the western
61 Amazon of Ecuador that indicate the Southern Oscillation Index (SOI), a measure of occurrence and strength of El Niño and La Niña, may be associated with major swings in species abundances when marked by La Niña events. Ideally, studies in the tropics and subtropics should report the SOI indices for the study period. Following that suggestion, the SOI values (available at http://www.cpc.ncep.noaa.gov/data/indices/soi) indicate no pronounced oscillation during our collecting period.
Altitudinal gradient
Carabid species assemblages appear to be strongly influenced by altitude in Neotropical
Peruvian cloud forests. Altitudinal zones were distinct in the ordination space , with only slight overlap between the 1500 m and 2000 m zones. Adjacent altitudinal zones along the gradient were no more than 52% similar. The 3400 m altitudinal zone, which was localized in the ordination space, is where cloud forest and elfin forest meet the puna alpine grassland ecosystem. Only one species was unique to this zone; the remaining seven species had altitudinal ranges that did not reach below 2500 m. Turnover in species composition along the altitudinal gradient is probably linked to the different environmental adaptations necessary for increasingly harsh abiotic environments and decreases in primary productivity (McCoy 1990; Escobar et al. 2005). Changes in tree species composition for this same gradient (Meier et al. 2010) are likely to influence the composition of carabid beetle assemblages, or at least point to the influence, such as different soil types. Changes in predation pressures could also possibly influence carabid beetle assemblages. In the K’osñipata Valley of southeastern Peru, where this study was conducted, birds and bats, both potential predators of carabid beetles, exhibit altitudinal differences in species composition (Patterson 1998). Although no potential biotic causal
62 agents are identified, dung beetle assemblages also vary significantly between high and low altitude locations in the Columbian Andes (Escobar et al. 2005).
Rarified richness of carabid beetles suggests that there could be a mid-elevation peak in diversity within the cloud forest zone (with Sr highest at the mid-elevation site,
2000m). The altitudinal zone 2000 m is situated just above cloud base in the K’osñipata
Valley, representing the approximate location of the ecotone between lowland forest and high Andean forest (Young and León 1999). The high beta diversity value indicates that these assemblages are relatively unique, with the highest dissimilarity (80%) for assemblages between 2000 m and 2500 m. A middle altitude peak in species richness has been reported for other Neotropical insect taxa, e.g., geometrid moths in Costa Rica
(Brehm et al. 2007), scarab beetles in the Colombian Andes (Escobar et al. 2005), ichneumonid wasps along the same gradient as this study (Castillo-Cavero 2009), and sweep samples of insects in Venezuela (Janzen et al. 1976). Moret (2009) also observed a mid-elevation peak in carabid beetle species within the alpine páramo ecosystem in
Ecuador, but like in the present study his lower elevation was not in the lowlands of
Amazonia. The mid-domain effect (MDE) has been offered as an explanation for the mid-elevation peak in species diversity (e.g., McCain 2007). The MDE predicts that species richness will peak at the middle of a bounded gradient because there is a higher probability that species will occur at the center of the gradient due to geometric constraints (Colwell et al. 2004). However, the MDE hypothesis may better explain patterns for data drawn from a more complete altitude gradient. For ground dwelling carabids, that should include sampling of beetle assemblages beginning in lowland
Amazonia, whereas in this study sampling did not occur at less than 1400 m. For example,
63 with more extensive search efforts, Erwin (1991) found more than 1000 ground dwelling and arboreal carabid species at Pakitza (Rio Manu, Peru); also, nearly 500 arboreal carabid species have been found from arthropod canopy fogging in the Yasuni area of
Ecuador (Erwin et al. 2005), with the ground fauna sampling still underway.
Although a middle peak in species richness has been documented for some
Neotropical taxa, a decreasing monotonic trend with altitude in species richness has also been reported, e.g., syntopic birds in Peru (Terborgh 1977), termites in Peru (Palin et al.
2011), and Neotropical tree communities (Gentry 1988). Raw species counts for carabid beetles used in this study also decrease monotonically (Maveety et al. 2011). Wolda
(1987) suggested that a linear trend in species richness may be linked to long term sampling while short term sampling is more likely to reveal a middle altitude peak.
Estimates of species richness by altitude may depend on the type and length of sampling employed. The present study was limited to one collection year on one transect and did not extend to the lowest altitudes. Given the range of altitude we sampled, which focused on the high altitude montane ecosystem, we cannot definitively predict the pattern of diversity if sampling was extended to the low point in the Amazon basin in
Manu National Park (approximately 300 m elevation). Sampling multiple transects spanning the entire altitudinal gradient would also be needed to obtain a complete picture of how species richness varies with altitude (Rahbek 1995). However, this study is the first systematic investigation of carabid beetles over an annual cycle and at multiple elevations of a tropical montane forest. The results indicate that tropical montane species assemblages change considerably with altitude and season. Additional studies are needed to document the full extent of these changes, and could be especially relevant in light of
64 the potential effects of climate change (Williams et al. 2007).
65 Acknowledgments
The Peruvian Ministry of Agriculture, Instituto Nacional de Recursos Naturales, and
Servicio Nacional de Áreas Naturales Protegidas por el Estado provided collection and export permits. We thank members of the Entomology Department at the Museo de
Historia Natural de la Universidad Nacional Mayor de San Marcos, especially Dr.
Gerardo Lamas who assisted with permit coordination and specimen loans. We also thank the Amazon Conservation Association (ACCA), PeruVerde, and ProNaturaleza for help with field logistics, and H.F. Jaquehua Callo, J.C. Ttito Quispe, and C. Chaparo
Zamalloa for field assistance. The Fulbright Program, Wake Forest University, and the
National Museum of Natural History at the Smithsonian Institution provided financial support.
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75 Figure Headings
Figure III - 1. Species accumulation curves for carabid beetles collected in the rainy season (Nov 07 – Apr 08) and the dry season (May – Oct 08) at elevations between 1400 and 3400 m at K’osñipata Valley, Manu National Park, Peru. Species numbers were estimated using the Mao Tau richness estimator. Vertical line represents a rarified sample size of 739 individuals; dashed lines represent 95% CI.
Figure III - 2. Number of carabid species collected at K’osñipata Valley, Peru, as a function of (A) species accumulation, using the Mao Tau richness estimator, for each altitudinal zone (the vertical line represents a standardized sample size where N = 172
[95% CI are not included for clarity]); and (B) rarified richness and altitude, adjusted by standardized sample size. Bars represent 95% CI.
Figure III - 3. Ordination by non-metric multidimensional scaling based on Sørensen’s
Index (Bray Curtis). Each data point represents the carabid beetle assemblage within an altitudinal zone (indicated by clusters). Black fill represents dry season month and gray fill represents rainy season months.
76
Figure III ‒ 1
77
Figure III ‒ 2
78
Figure III ‒ 3
79
CHAPTER IV
EFFECT OF DISTURBANCE AND INTER-ANNUAL VARIATION ON CARABID
BEETLE ASSEMBLAGES IN AN ANDEAN CLOUD FOREST
The following manuscript will be submitted to Journal of Tropical Ecology (12/2013).
Stylistic variations are due to the requirements of the journal.
80 Abstract
The diversity and community structure of carabid beetle assemblages were examined along both a disturbed and an old growth altitudinal gradient in Manu Biosphere Reserve, southeastern Peru. Carabid beetles were collected by hand from approximately 2000 m to
3500 m for both gradients at three census intervals: 2008, 2010 and 2011. There was no significant trend with altitude for raw species number, rarified species richness, or diversity metrics (Shannon-Weiner, Fisher’s alpha) and community metrics (Shannon’s evenness, probability of interspecific encounter). Diversity and community indices were usually higher for the old growth gradient compared to the disturbed gradient, both within altitudinal zones and for the entire gradient. A reduction in species richness with disturbance would be expected because of the reduced available habitat. Both old growth and disturbed gradients had similarly even assemblages, but varied markedly by composition (assessed using non-metric multidimensional scaling) with an average similarity of 40% between the gradients. There was no inter-annual difference in species richness or composition for either gradient, however there was up to 50% species turnover between census intervals. Future collections would be useful to document changes in carabid beetle richness and community structure on a longer time scale.
Keywords: altitudinal gradient, Carabidae, cloud forest, disturbance, multi-year study,
Neotropics, NMDS, puna, rarefaction, species richness
81
Introduction
The tropical Andes constitute a biodiversity hotspot (Myers et al. 2000), supporting exceptionally high levels of biodiversity and endemism for numerous taxa (Bush et al.
2004, Foster 2001, Patterson et al. 1998). The eastern slopes of the Andes from ca. 2000 meters a.s.l to 3500 meters a.s.l., are regularly immersed in clouds (Kricher 1997), creating the specialized cloud forests that occur across the Andean landscape (Foster
2001). Frequent cloud cover is crucial to the functioning of the cloud forest ecosystem and the organisms it supports (Lawton et al. 2001). Tropical montane cloud forests are essential for ecosystem processes, contributing to the hydrological cycle (Armenteras et al. 2011) and protecting against erosion in steep high altitude terrain (Ataroff and Rada
2000).
Tropical montane forests are especially prone to both natural and anthropogenic disturbance. Natural disturbance occurs due to steep slopes and high elevation (Young
1994), resulting in slope instability and landslides (Kessler 1999, Lozano et al. 2005).
However, forest degradation and fragmentation due to anthropogenic disturbance are major threats to tropical montane cloud forests, especially in the Andes (Erwin & Geraci
2009, Oliveira et al. 2007, Perz et al. 2008). Human land use, e.g., logging, agriculture, ranching, and road construction, has resulted in reduced forest cover (Erwin & Geraci
2009, Perz et al. 2008). Forest degradation can result in decreased cloud cover and increased insolation (Malhi et al. 2008), which may have a negative impact on organisms adapted to these cool moist cloud forests (Foster 2001). In fact, changes in precipitation may be one of the more critical consequences of deforestation (Malhi et al. 2008). In cloud forests, the moisture provided by buffering clouds is crucial for water balance,
82 providing up to 37% of moisture (Bush et al. 2004) and in the Andes cloud forests play an important role in watershed hydro-dynamics and protection against erosion
(Armenteras et al. 2011, Ataroff & Rada 2000).
Anthropogenic pressure on tropical montane forests of the Andes dates back to pre-Colombian civilizations (Young and León 1999, Armenteras et al. 2011). On the eastern slopes of the Andes in southern Peru, some evidence still exists of pre-Colombian agricultural terracing below 1500 m, most likely for coca cultivation (Young and León
1999). The optimal zones for agriculture are just outside the range of the cloud forest belt, from about 500 m to 1200 m, and above timberline (Nogués-Bravo et al. 2008, Terborgh
1977) from ca. 3500 m upward (Young and León 1999). The clearing of tropical lowland forests for agriculture, especially upwind of cloud forests, has a significant impact on altitudinal level of cloud base (Lawton et al. 2001). At the upper end of the cloud forest belt, timberline in the high Andes has a history of human alterations (Sarmiento &
Frolich 2002, Young 2008), including agricultural clearing and fires, such that current tree line is likely much lower than that expected for an undisturbed state (Feeley &
Silman 2010).
The building and expansion of roads in Andean cloud forests has caused significant environmental changes in the Andean landscape (Schjellerup 2000). There is an obvious causal relationship between road construction and deforestation (Mäki et al.
2001); however, the building of road networks is important for development in many
Amazonian countries (Young 1994). Roads facilitate the access of humans to natural resources and of rural producers to markets (Perz et al. 2008). Nonetheless, roads degrade stream networks, fragment habitats, foster spread of exotic species, cause wildlife
83 mortality and species loss (from construction and collision with vehicles), may catalyze local climate change, and increase local human use of forest (Trombulak & Frissel 2000,
Perz et al. 2008). Increased human use caused by road presence may result in local colonization (leading to clearing of forest for pasture, agriculture) or uncontrolled extraction of timber (Young 1994, INRENA 2003), increasing the natural instability of mountain zones (Young 1994).
The impact of road construction and the associated landscape changes on insect species richness and community structures is largely unknown in tropical forests (Brehm
& Fiedler 2005, Nichols et al. 2007). Although insects represent approximately 80% of recorded life on earth (Erwin 1996), arthropod studies in the tropics are underrepresented, at least partly due to difficulty in accurately sampling (Brehm et al. 2007). Surprisingly, few studies of insect diversity have been conducted in the montane forests of the Andes
(Brehm & Fiedler 2005). Insects are strongly affected by disturbance and landscape changes, but are overlooked for disturbance studies (Nichols et al. 2007). For highly diverse taxonomic groups, such as insects, obtaining an exhaustive or near exhaustive sample in the tropics has been a serious challenge; in addition, a large proportion of the species are seemingly rare, leading to statistical challenges in data analysis (Brehm &
Fiedler 2004).
The purpose of the present study is to examine carabid beetle (Coleoptera:
Carabidae) assemblages in relation to anthropogenic disturbance caused by a road along an altitudinal gradient in the K’osñipata Valley of the southeastern Peruvian Andes.
Carabidae is one of the most diverse taxonomic beetle families (Niemelä 1996). Carabid beetles are generally easy to collect, prepare, and describe (Erwin 1996), vary widely in
84 structural attributes, behavior, and ecology, and can successfully signal environmental change (Niemelä et al. 2000, Kotze et al. 2011), making them a desirable model for biodiversity studies (Erwin 1996, Rainio & Niemelä 2003). Species richness and carabid beetle community composition between a disturbed and old growth gradient were analyzed along an altitudinal gradient. We characterize the history of disturbance along the cloud forest portion of the road that runs from Cusco to Pilcopata, just outside of
Manu National Park (MNP), and compare this to an old growth gradient within MNP. We address the difference in species richness between the disturbed and old growth forest gradients, and examine whether the assemblages of two gradients are compositionally similar.
Since this is one of the few studies of tropical insects based on relatively large data sets that sample more than one year of data, inter-annual changes in diversity and species composition can also be estimated. One of the less studied aspects of insects is temporal dynamics (Grimbacher and Stork 2009), due to the large taxonomically difficult data sets and field logistics. Seasonality affects carabid beetles in the tropics (Lucky et al.
2002, see also Chapter III / Maveety et al. in press), but little is known about multi-year variation. We examine to what extent multi-year collections play a role in the richness and composition of carabid beetle assemblages.
85 Methods
Disturbed vs. old growth gradients
Two altitudinal gradients were sampled along the eastern slope of Andes, in the
K’osñipata Valley, Province of Paucartambo, Department of Cusco, Peru: an old growth
(OG) gradient and a disturbed (D) gradient. The OG gradient follows an old Incan footpath (Trocha Union) that has experienced only foot traffic. The Trocha Union runs through Manu National Park (MNP) (the largest reserved area in Peru, established in
1968, IUCN 2008), and is a fairly inaccessible path cutting through difficult terrain
(Girardin et al. 2010). The gradient extends from 3650 m, above timberline in the alpine puna, to 1850 m, just above cloud base, over a distance of nine aerial km (with an average decrease of 200 m in altitude km-1). Collections on the OG gradient were carried out at four altitudinal zones, which are part of the plot system established by Andes
Biodiversity and Ecosystem Research Group (ABERG,
(Table 1, Figure 1). Along the old growth gradient, the most common tree family is
Cyatheacea (tree fern, Garcia Cabrera 2011). Within zone C (2750 m – 3000 m, see Table
1), the dominant families are Clusiaceae, Cunoniceae, and Lauraceae and within zone A they are Clusiaceae, Alzateaceae, Clethraceae, and Myrtaceae (Girardin et al. 2010).
The D gradient, which is approximately parallel to the OG gradient, follows the
Cusco-Pilcopata highway, a dirt road whose construction was completed in the 1960s.
Although this road is contained within the buffer zone of the Manu Biosphere Reserve
(Figure 1, Cultural Zone), there is continuous disturbance associated with vehicular traffic e.g., air and human pollution, increased landslides, and occasional road maintenance (see Appendix for characterization of disturbance in K’osñipata Valley).
86 The D gradient was sampled from 3450 m to 2000 m at four altitudinal zones, over 11 km aerial distance (with an average decrease of 132 m in altitude km-1) (Table 1, Figure 1).
Location data for both gradients are listed in Appendix Table A1. Table 2 outlines a description of the collection sites for the D gradient, including type of disturbance. There is an apparent difference of decreased cloud cover and precipitation, and increased temperature, at any altitudinal zone on the disturbed as compared to the old growth gradient (pers. obs.).
The D gradient was sampled monthly in 2008 during dry season months (May –
July). Both D and OG gradients were sampled in 2010 and 2011 during the dry season months (Jun.‒Aug.). In order to compare the most similar data sets for gradient comparison, only the beetles collected during 2010 and 2011 were analyzed (i.e., the OG gradient was not collected during 2008). However, samples from all collection years,
2008, 2010, and 2011, were used for inter-annual analysis.
Collections of Carabidae
Carabid beetles were collected by hand searches, which consisted of sifting through leaf litter on the ground, and examining vegetation up to 1.5 m in height. Along the OG gradient, beetles were collected under the closed forest canopy; along the D gradient, beetles were collected along the road and forest edge. Due to the nocturnal behavior of carabid beetles, searches took place at night. Collections at lower altitudes started between 20:00 to 21:00, but at higher altitudes where the temperature can drop to nearly freezing by that time, searches began directly after sunset. Search effort continued until at least 100 individuals were collected, or until eight person-hours of search effort were completed. Table A3 (Appendix) contains details of search effort. Hand collections only
87 sample the epigeic, or surface dwelling, carabid beetles; consequently certain carabid taxa, e.g., hypogean and arboreal beetles, will be underrepresented from hand sampling techniques. Because there were no previous collections from the area and there are limited taxonomic descriptions of Andean carabid beetles, specimens were identified to morphospecies level. In areas of extreme diversity, morphospecies identification can lead to reliable estimations of species richness (Oliver & Beattie 1996, Brehm et al. 2007).
Data analysis
Because of the variable number of individuals collected per sampling effort, comparisons of raw species number may be misleading. Due to their extremely high diversity, this is a common problem when analyzing the data of tropical arthropod species richness, but can be avoided by interpolating, or rarifying, samples via smoothed species accumulation curves (Gotelli & Colwell 2001, Gotelli 2004). Rarefaction is commonly reported in the literature for tropical insects, e.g., geometrid moths in Ecuador (Brehm et al. 2003) and
Costa Rica (Brehm et al. 2007), and dung beetles in Mexico and Colombia (Escobar et al.
2007). We employ the Mao Tau richness estimator for rarefaction of species diversity, a nonparametric estimator of species richness, with sample based species accumulation curves generated from EstimateS V9.0 (Colwell 2013). Species accumulation curves were calculated with collection date as a replicate, and data were randomized 500 times.
We also report the extrapolated estimate of species diversity, asymptote of S for the observed assemblage, using the non-parametric Chao 2 estimator from EstimateS (Gotelli
& Ellison 2013). The difference between means of richness estimators was compared using p-values calculated in R 2.13.1
88 alpha) and community metrics (Shannon’s Evenness, Probability of Inter-specific
Encounter [P.I.E.]) and dominance (Berger-Parker Index) were calculated for gradient (D vs. OG) and inter-annual comparisons according to Magurran & McGill (2011). Rarity was also estimated for D vs. OG and inter-annual comparisons; a rare species was defined as ≤ 1% of the individuals collected. All diversity and community metrics were tested for correlation with altitude by regression in Microsoft Excel.
To answer the question of how disturbance affects assemblage composition, three parameters were examined: beta diversity, ordination of assemblages and assemblage structure (as measured by evenness). Beta diversity was calculated with Sørensen’s dissimilarity index, β = (b + c) / (2a + b + c), where a is the number of shared species between comparable zones, and b and c are the number of unique species. Beta diversity was calculated in two ways: a) between D and OG for each altitudinal zone, and b) between adjacent altitudinal zones for each gradient. Sørensen’s similarity index ranges from 0 to 1, with the most dissimilar assemblages approaching a value of one (Magurran
& McGill 2011). In both cases, we distinguished between changes in species composition across sites by replacement or by loss of species following beta diversity partitioning of
Baselga (2010). Total beta diversity, as described above based on Sørensen’s dissimilarity index (βsor), can be partitioned into contributions by turnover (Simpson’s dissimilarity, βsim) and nestedness (species loss, βnes).
Data were ordinated by non-metric multidimensional scaling (NMDS), using
PCOrd Version 4
89 six axes (from 400 iterations, 40 runs with real data and 50 randomized runs) (McCune et al. 2002). Previous work suggests that for tropical arthropods other ordination methods
(canonical analysis and detrended correspondence analysis) depict similar patterns to those found for NMDS (Brehm & Fiedler 2004). Carabid beetle assemblages were further analyzed using relative abundance plots and ordination. Relative abundance plots describe changes in community structure and evenness, specifically in terms of common and rare species. Relative abundance was calculated as a percentage of the total sample and plotted on a log scale.
To examine turnover between the different years of collection, temporal turnover was calculated as t = (b + c) / (S1 + S2), where b and c are the number of species unique to each census, and S1 and S2 are the total number of species present in either census (see
Magurran & McGill 2011). Temporal turnover was calculated a) between years at each altitudinal zone and b) between years for the entire gradient. The temporal turnover index also yields values from 0 to 1, with values approaching 1 indicating higher dissimilarity in species composition, i.e., higher turnover.
90 Results
Species richness and community composition in disturbed vs. old growth gradients
Comparisons between the D and OG gradients were based on the 2010 and 2011 collections, which consisted of 1,331 individuals representing 64 morphospecies (Table
1). Although a greater number of individuals were collected on the D gradient, the raw number of species was similar for both gradients (SD = 41, SOG = 39) (Table 3). None of the diversity or community indices calculated in Table 3 were significantly correlated with altitude, nor exhibited significant differences between D and OG within altitudinal zones, probably due to the limited statistical power associated with only four altitudinal zones. However all diversity metrics were consistently higher for the OG gradient than the D gradient (Table 3). Dominance, where a higher value reflects low diversity, was higher on the D gradient.
Of the 64 species collected, 21 species (33%) occurred only on the OG gradient,
25 species (39%) occurred only on the D gradient, and 18 species (28%) were found on both gradients. For the D gradient, there were 14 (29%) singleton species and 27 (66%) rare species. For the OG gradient, there were 15 (47%) singleton species and 26 (67%) rare species (Table 3). The majority of species for both gradients (S = 49, 77%) occurred at only one altitudinal zone. A similar proportion of species occurred in just one altitude zone for the D gradient (39%, 25 species) and the OG gradient (36%, 23 species).
Rarified richness (Sr) was approximately 50% higher for the OG gradient (Figure
2, rarified at n = 463, p = 0.014). Neither of the species accumulation curves reached an asymptote, indicating that sampling of carabid species for both D and OG was not exhaustive. The Chao 2 richness estimator reported approximately the same number of
91 extrapolated S: 137 ± 62 (x¯ ± SD) species for D gradient and 137 ± 56 species for OG gradient (P = 0.50). There was no significant correlation between altitude and Sr for either the D or the OG gradients (Figure 3, rD = 0.054 and rOG = 0.72, p > 0.05). However, for both gradients, differences in Sr were always significant between adjacent altitudinal zones, p ≤ 0.0042, except for zones 3000 m = 3500 m on the D gradient, p = 0.079. There was no significant difference in Sr between D and OG for any altitude zone (Figure 3) except for 2000 m where OG had a higher Sr than D, p = 0.0046.
The overall similarity in species composition between the two gradients was 40%.
Beta diversity decreased between the D and OG gradients with increasing altitude, but not significantly (r = 0.88, d.f. = 2, p = 0.12, Figure 3), probably due to low statistical power associated with just four data points. Species turnover appears to be the largest contributing factor to beta diversity (as measured by βsim) with species loss (as measured by βness) constituting a negligible part of beta diversity (Table 4). Beta diversity between adjacent altitudinal zones (not illustrated) showed similar patterns for both the D and the
OG gradient, with the greatest similarity in species composition at mid-altitude between the 2500 m and 3000 m zones. Species loss, or βness, constituted a small part of total beta diversity between altitudinal zones.
Carabid beetle assemblages for the D and OG gradients varied in composition
(NMDS, Figure 4). Axes 1 and 2 explained 38.1% of variance (axis 1: r2 = 0.175, axis 3: r2 = 0.206). On axis 3, OG gradient sites were all markedly lower than D gradient sites, with the exception of the highest altitude OG site at 3650 m, which is above timberline in the puna, with this value clustering with those found for the D gradient. Otherwise, there was no altitudinal trend in composition for either the D or OG sites.
92 Relative abundance curves (Figure 5) for both D and OG had relatively long right hand tails, reflecting a large proportion of rare species. At the left end of the curve, the most abundant species was two times more abundant on the disturbed gradient (33%) than the old growth gradient (16%). Otherwise, the two curves show similar evenness.
Inter-annual comparison
For inter-annual comparisons, 2,034 individuals were collected, representing 73 morphospecies. Rarified species richness, adjusted at n = 590, was 30 ± 3.7 (x¯ ± SD) in
2008, which was significantly less than both 2010 (45 ± 5.7, p = 0.014) and 2011 (43.5 ±
4.0, p = 0.008), but there was no difference in Sr for 2010 and 2011, p = 0.42. There was also no difference between years for the Chao 2 richness estimator: (x¯ ± SD) in 2008 S =
59 ± 15, in 2010 S = 181 ± 84 and in 2011 S = 92 ± 22, with P ≥ 0.07 for all comparisons.
There was no difference between sequential collection years on the D gradient (Figure 6); however 2011 was more species rich than 2008 (p = 0.0034). On the OG gradient, there was no difference in species richness between years. The OG gradient was more species rich in 2010 than the D gradient (p = 0.020), but there was no difference in 2011 (p >
0.05, Figure 6). No diversity metrics (Table 5) were significantly different among years, although all values were less for 2008. Dominance was the greatest during 2008, but there was no significant difference among years. During 2008 19 (58%) rare species were collected, while in 2010 and 2011 28 (62%) and 36 (72%) rare species were collected, respectively.
There was 46% temporal turnover in morphospecies composition between 2008 and 2010, 37% turnover between 2010 and 2011, and 54% turnover for the more extended period from 2008 to 2011 (Table 6). There was no significant correlation for
93 temporal turnover by altitude. Relative abundance plots showed similar degrees of community evenness among the three different collection periods (not shown but similar to pattern seen in Figure 5). NDMS analysis (Figure 7) suggests that species assemblage compositions among the three collection periods were random, with no discernible pattern by collection year. In contrast, collections from altitudinal zones approximately sorted according with disturbance level, with D sites clustering on the low end of the x- axis (axis 2) and OG sites on the high end. Axes 2 and 3 explained 42.6% of variance (2: r2 = 0.221, 3: r2 = 0.205).
94 Discussion
The present analyses found no evidence that carabid species richness in the Andes is correlated with altitude within the cloud forest zone. Similar results have been reported for mice on the same altitudinal gradient as the present study (Patterson et al. 1998) and for geometrid moths along an altitudinal gradient in Ecuador (Brehm et al. 2003). Lack of correlation between species richness and altitude has more often been reported for organisms that operate on a more fine grain scale, i.e., fungal wood decomposers (Meier et al. 2010) and microorganisms that follow pH more than climatic variables (Fierer et al.
2011). However, when examining the same D gradient from 1500 m to 3450 m, Maveety et al. (2011) found a negative linear trend in raw species number and altitude in carabid beetles. When rarified by sampling effort, there was a mid-altitude peak in richness at
2000 m on the same D gradient range (Chapter III / Maveety et al. in press). Differences observed between the latter results and the present study may reflect the scale of rarefaction (in Chapter III / Maveety et al. in press species richness was rarified at n =
163 whereas the present study rarified at n = 50). Furthermore, the gradient of this study was more limited than that of Chapter III / Maveety et al. in press. We examined the richness of carabid beetle assemblages at the local scale, but observing richness patterns at the level of regional diversity may be necessary to elucidate true patterns of altitudinal species richness (Ricklefs 2008).
Species richness and diversity and community indices, both within altitudinal zones and for the entire gradient, were usually higher for the OG gradient than the D gradient. However, differences were not always significant, which may be due in part to the naturally high degree of disturbance present on the OG gradient due to landslides
95 associated with the steep slopes (Kessler 1999). Decreased diversity with increased disturbance has been reported for arthropods inhabiting the microhabitats of epiphyte mats in Neotropical cloud forests (Yanoviak & Nadkarni 2001), beetles in Cameroon
(Lawton et al. 1998), geometrid moths in Ecuador (Brehm & Fielder 2005), and dung beetles in the Colombian Andes (Escobar et al. 2007, Medina et al. 2002). There is some evidence that elevation specialists are less common in forests bordering roads, where generalist species are instead often found (Young 1994). A reduction in species diversity with disturbance may also be expected because of the reduced available habitat, which may be increasingly relevant as forest areas are threatened by anthropogenic activities.
Although less species rich, the D gradient supported a carabid beetle assemblage distinct from the OG assemblage, mostly likely due to species turnover than species loss, as indicated by partitioned beta diversity (Baselga 2010). Dunn (2004) suggests that 20-
40 years after regeneration, secondary forests tend to show diversity recovery (by number of species) but species composition recovers at a slower rate. In addition, roadside modification may support species that prefer open habitats (Trombulak & Frissel 2000).
The dominant tribe on the D gradient, Harpalini, is an herbivorous seed feeder with a robust body plan (Kotze et al. 2011). This group often feeds on grass seeds that are in high abundance on the disturbed roadside (T.L. Erwin, pers. comm.). Two tribes were unique to the D gradient. The first, Odacanthini, is often associated with grass and grass- like plants (Erwin 1979), while the second, Lachnophorini, usually occurs in open areas and drier habitats (Erwin 2004). Carabid beetles are often limited by low humidity (Lövei
& Sunderland 1996, Kotze et al. 2011), and disturbed sites tend to be warmer and drier than old growth forests (Larsen 2012), further driving compositional differences. Carabid
96 beetles had greater average body length on the D gradient (Chapter V), which is potentially adaptive to prevent desiccation in the drier and arid conditions typical of a disturbed habitat (Larsen 2012, Schoener & Janzen 1968). The dominant tribe on the OG gradient, Bembidiini, is a taxon of relatively small-sized adults, on average no longer than 5 mm (see table A5, appendix), and was represented exclusively by Bembidion, a typical high altitude genus in South America (Erwin 1979). While Bembidion species are found on the D gradient, species of this genus are almost three times more abundant on the OG gradient. The tribes Scaratini (a taxon with fossorial adults), represented by only
2 singleton species, and Galeritini (whose adults are large predators and fast runners)
(Erwin 1979) were found only on the OG gradient.
Species turnover decreased between the two gradients as altitude increased, as indicated by decreasing beta diversity. Interestingly, the top altitudinal zone on the OG gradient (3650 m) grouped with the anthropogenically disturbed D gradient sites in ordination space, also indicating greater similarity. The highest OG site is situated at
3650 m above timberline in the puna ecosystem. The puna has a history of anthropogenic disturbance by agriculture, cattle grazing, and fire (Sarmiento & Frolich 2002), and therefore it is not surprising that it clusters with the anthropogenically disturbed gradient sites.
There was little difference in the distributions of carabid beetle abundances between the D and OG gradients, as shown by the relative abundance plots. The shape of the carabid beetle species assemblage curve is similar to the log normal pattern predicted for a tropical community by neutral theory (Hubbell 2001). However, Pitman et al.
(2001) suggest that species composition of tree communities in western Amazonia have
97 more deterministic components (i.e., niche assembly) when examined at the landscape scale. Results from rank abundance distributions of ichneumon wasps collected from malaise trapping on the same D gradient used in this study (Castillo-Cavero 2009) and tree communities from 1 ha. plots on the same OG gradient used in this study (M.R.
Silman, pers. comm.) illustrate more of a species rich and heterogeneous assemblage that conforms to the log-normal shape; in comparison to those studies, carabid beetle assemblages more closely resemble log-series. Additional abundance data need to be collected to reveal a more accurate pattern of commonness and rarity.
The 2008 census was significantly less species rich than 2010 and 2011; however only the D gradient was sampled during the 2008 census. Adding an additional gradient increased species richness of the carabid assemblage, especially with the overall greater richness of the OG gradient. Although up to 54% species turnover between any two census intervals implies a change in carabid beetle composition, NMDS ordination did not support this, with no discernible pattern in ordination space. Additional collections are needed to document changes in carabid beetle diversity and community structure on a longer time scale.
Because of the potential compounding factors of climate change the full effects of anthropogenic disturbance on the D gradient are uncertain (Larsen 2012, Laurance et al.
2011, Perz et al. 2008). It is important to establish baseline surveys and document changes in species distribution as communities shift in altitude and potentially disappear, especially for tropical montane organisms that are at greater risk of extinction (Williams et al. 2007). The more baseline data available, the better we are able to plan for conservation (Erwin & Geraci 2009). There are methodological challenges associated
98 with documenting tropical arthropod communities, i.e., incomplete sampling and high proportion of rare species (Brehm et al. 2003), both of which occur in this study. Future studies with sampling at increased time intervals will be necessary to evaluate potential climate related changes, such as upslope migration, in the carabid fauna.
99 Acknowledgements
Financial support was provided by the Fulbright Program, National Museum of Natural
History at the Smithsonian Institution, the Entomological Society of America, and Wake
Forest University. Collection and export permits were obtained from the Peruvian
Ministry of Agriculture (Instituto Nacional de Recursos Naturales and Servicio Nacional de Áreas Naturales Protedigdas por el Estado), with the help of the Entomology
Department at the Museo de Historia Natural de la Universidad Nacional Mayor de San
Marcos. We thank the Amazon Conservation Association, PeruVerde, and ProNaturaleza for logistical support. A special thanks to R Hillyer and A Tejedor for help with history of the Cusco-Pilcopata road, M.R. Silman for tree data from the OG gradient, and to T.L.
Erwin for help with carabid beetle identifications.
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Collection Altitude Description and dominant Type References Site (m) vegetation Disturbance Historic: Sarmiento & Frolich P.V. Puna and elfin forest agriculture, 3450 2002, Patterson et al. Acjanaco Poaceae (bunchgrasses) grazing pasture, 2006 and fires Low stature cloud forest, high epiphytic growth. Patterson et al. 2006, Wayqecha Canopy height approx. 15 m, with Open habitat from Girardin et al. 2010, Biological 3000 25% opening. road disturbance Ignatov et al. 2011, Station Weinmannia; Clusia; Sulca Garro 2011 Hesperomeles; Melastomataceae; Ericaceae Medium stature cloud forest; steep terrain. Small settlement, Pillahuata 2500 Road switches back approx. 3 Patterson et al. 2006 agriculture times creating very dry environment Agriculture Tall stature cloud forest, rocky (rocoto peppers), INRENA 2003, Rocotal ground. 2000 illegal logging, Patterson et al. 2006, (Suecia) Canopy height approx. 20 m, with prone to Sulca Garro 2011 20% opening. landslides 113 114 Table IV – 4. Partitioned beta diversity (β) by altitude: index of total β (Sørenen’s Index), turnover (Simpson’s Index), and species loss (Nestedness Index). Altitudinal Sørenen’s Index Simpson’s Index Nestedness Index Zone (βsor) (βsim) (βness) A 0.913 0.909 0.004 B 0.600 0.556 0.044 C 0.515 0.500 0.015 D 0.500 0.500 0.000 115 Table IV - 5. Number of individuals (n) and species (S) and diversity and community metrics for the different collection years: H’ (Shannon-Weiner), α (Fisher’s alpha), J’ (Shannon’s evenness), PIE (probability of interspecific encounter), Dominance (Berger- Parker Index), and percent singletons. Year n S H' α J' PIE Dominance % Singletons 2008 700 33 2.18 7.19 0.62 0.85 0.30 30 2010 584 45 2.75 11.33 0.72 0.88 0.27 36 2011 750 50 2.77 12.05 0.71 0.9 0.22 38 116 Table IV - 6. Index of species temporal turnover (t) by collection year. t Altitude (m) 2008 vs. 2010 2008 vs. 2011 2010 vs. 2011 2000 0.47 0.53 0.44 2500 0.64 0.67 0.33 3000 0.50 0.56 0.25 3450 0.86 0.60 0.33 Total 0.46 0.54 0.37 117 List of Figure Headings Figure IV - 1. Map of study area in Manu Biosphere Reserve, Peru. Figure IV - 2. Species accumulation (Mao Tau richness estimator) for the old growth and disturbed gradients. Dashed lines represent 95% confidence intervals. Figure IV - 3. Rarified species richness (Mao Tau) by altitudinal zone for the old growth and disturbed gradients. Bars represent 95% confidence intervals. Dashed line represents the beta diversity (Sørensen’s dissimilarity index) between adjacent altitudinal zones for both the D and OG gradients (secondary y-axis). Figure IV - 4. Non-metric multidimensional scaling (Bray Curtis) comparing old growth and disturbed altitudinal zones. Figure IV - 5. Relative abundance plots for the disturbed and old growth gradients. Figure IV - 6. Species richness rarified at n = 151 (Mao Tau richness estimator) for the three different collection years between the D and OG gradient. Bars represent 95% confidence intervals. Figure IV - 7. Non-metric multidimensional scaling (Bray-Curtis index) based on interannual comparisons. Shaded symbols represent old growth gradient altitudinal zones and empty symbols represent the disturbed gradient. 118 Figure IV – 1 119 Figure IV – 2 120 Figure IV ‒ 3 121 Figure IV ‒ 4 122 Figure IV ‒ 5 123 Figure IV ‒ 6 124 Figure IV ‒ 7 125 Appendix History and type of disturbance in K’osñipata Valley In 1951, entomologist Felix Woytkowski described the road of the K’osñipata Valley as “wind[ing] over the rock ledges, rocks, along sharp bends … The road was so narrow that the four wheels of the truck could hardly find enough space to cling to it… This was an ordinary journey over the rocky, terrifying Andean Cordilleras” (Woytkowski 1978, pg. 155-156). Inca roads extended into the steep montane terrain of the K’osñipata region for trade between the communities of the Andes and Amazon in the pre-Colombian era; after Spanish colonization, coca plantations, gold mines, and trading posts were maintained in the area (Shepard et al. 2010). The rubber boom of the late 19th century (1895 to 1917) brought more traffic into the K’osñipata region (Shepard et al. 2010). The construction of the current condition of the road (Carretera Cusco-Pilcopata) in the K’osñipata region began around 1912 (A. Tejedor, pers. comm.) and was finalized in the 1960s by engineer Sven Ericsson (Woytkowski 1978, Young and León 1999). Government incentive programs encouraged settlers to develop haciendas, or plantations, on the eastern slopes of Peru in the early 1900s (Young and León 1999), which led to agricultural efforts alongside the road (including Zone A, B, and most likely C, of the D gradient). The Agrarian Reform of the early 1970s dissolved most of these haciendas, and split the area into many small land holdings (Young and León 1999); presently, different sections along the road of the cultural zone of MNP are privately owned by different non- government organizations such as Amazon Conservation Association (Zone C), ProNaturaleza (Zone B), and Peru Verde (just below Zone A, San Pedro, 1400 m). Over 126 the past 40 years, the K’osnipata Valley has been selectively logged (Merkord 2010), and at least illegally so in the 2000 m zone of the present study (Rocotal, INRENA 2003). 127 CHAPTER V PATTERNS OF CARABID BEETLE (COLEOPTERA: CARABIDAE) MORPHOLOGY ALONG A NEOTROPICAL ALTITUDINAL GRADIENT IN PERU The following manuscript was submitted to Ecological Entomology (8/2013). Stylistic variations are due to the requirements of the journal. 128 Abstract 1. Body length and dispersal ability were examined for carabid beetles (Coleoptera: Carabidae) sampled on an old growth and an anthropogenically disturbed altitudinal gradient in the Peruvian Andes. Dispersal ability was estimated by flight wing condition (i.e. macropterous or brachypterous) and the cuticular length of the flight muscle (medial length of the metasternum). 2. The relationship between body length and altitude for combined gradients varied by tribe, with all possible relationships found: positive, negative and no relationship. At the family level, a negative relationship between altitude and insect body length was found for carabid beetle assemblages, which was predicted due to decrease in resource diversity, habitat area, primary productivity and the increase in the unfavorable environment observed at high altitudes. 3. Flight muscle length was also highly variable among tribes, but a negative trend with altitude was found at the family level for combined gradients. Some tribes were either completely macropterous or brachypterous, but percentage brachyptery increased with altitude at the family level. We suggest two hypotheses that may explain the increased incidence of flightlessness observed with increasing altitude: a decreased need for dispersal potential and energetic constraints. 4. At the family level, carabid beetles tended to have a greater body length and decreased brachyptery on a disturbed gradient, compared to the old growth forest gradient. Increased dispersal ability was expected due to the need to find suitable habitat in disturbed areas. 129 5. Since carabid beetle morphology was highly variable by lineage, the results indicate that for the Andean altitudinal gradient the relationship between altitude and wing state is complex. However, there is a tendency for both reduced body size and dispersal ability with increasing altitude. Observed relationships may depend upon which tribes are examined and whether the forest on an altitudinal gradient has been disturbed. Key Words. Body size, brachyptery, cloud forest, dispersal ability, elevation, ground beetles, puna, wing state. 130 Introduction Questions about relationships between species diversity and physical gradients have traditionally focused on richness estimators and community composition (e.g. Terborgh 1977; Brehm et al. 2003). However, an examination of changes in morphological characters on gradients can also yield significant ecological and evolutionary insights. Studies on tropical altitudinal gradients are of particular interest due to the potential changes associated with regional and global climate change (Williams et al. 2007). Increasing altitude leads to increasing habitat stability and persistence (Roff 1990), decreasing habitat heterogeneity (Kavanaugh 1985, Brehm et al. 2003) and an increasingly unfavorable environment (McCoy 1990). As altitude increases, temperature and partial pressure of respiratory gasses decrease as precipitation and wind velocity increase. These factors contribute to a harsh, limiting abiotic environment (Hodkinson 2005), which may influence the diversity and composition of high altitude organisms (Mani 1968; Hodkinson 2005). They also may affect two morphological characters, body size and wing state, which are critical to the dispersal of many insects such as beetles (e.g., Lövei & Sunderland 1996; Gutiérrez & Menéndez 1997). In the literature, the relationship between altitude and insect body size is not consistent. Body size increases with altitude in weevils (Ectemnorhinini) (Chown & Klok 2003) and queen bumblebees (Bombus festivus) (Dillon et al. 2006), a trend that has been shown to follow temperature differences when resources are not limited (Smith et al. 2000; Hodkinson 2005). However, a decrease in insect body size with altitude has been reported for the majority of studies, e.g. the striped ground cricket (Allonemobius socius) (Mousseau 1997), worker bumblebees (Bombus festivus) (Dillon et al. 2006), flower- 131 head-feeding fruit flies (Tephritidae) (Kubota et al. 2007), dung beetles (Phanaeini) (Herzog et al. 2013), a carabid species, Carabus tosanus (Tsuchiya et al. 2012), and in general surveys of insect communities (Janzen et al. 1976; Guevara & Avilés 2013). In some cases, no relationship has been found, e.g. butterflies of Costa Rica (Hawkins and deVries 1996) and geometrid moths in Ecuador (Brehm & Fiedler 2004). To add to the confusion, both positive and negative correlations have been reported along an altitudinal gradient within a species, e.g. silphid beetle, Nicrophorus investigator, in the Colorado Rockies, (Smith et al. 2000). Clearly, more work is needed and one of the goals of this study is to determine the relationship between body size and altitude in Neotropical carabid beetles. The question of why flightlessness occurs has been of long standing interest (e.g. Darwin 1859; Darlington 1943). Since wings are not only important for flight but also courtship, crypsis, mimicry, hunting, escape, and dispersal (Hammond 1979; Wagner & Liebherr 1992), the evolution of flight is possibly the most important adaptation accounting for the success of insects (Ikeda et al. 2012). Yet, the loss of flight has evolved in nearly all insect orders, and repeatedly so in the family Carabidae (Harrison 1980; Kavanaugh 1985, Roff 1990, Lövei & Sunderland 1996, Harrison & Roberts 2000). Carabid beetles (Coleoptera: Carabidae) are useful as model organisms for ecological studies. They are a highly diverse taxon (Erwin 1996), are relatively easy to collect by active and passive methods, have well known biology, and are relatively easy to identify (Lövei & Sunderland 1996). As ectotherms, insects are especially useful models to study morphological changes because of their sensitivity to changes in the abiotic environment (Dillon et al. 2006). Carabid beetles are ideal for study of flight condition because of a 132 high variation of dispersal ability both within and among species, with both short and long winged forms (Gutiérrez & Menéndez 1997). Carabid beetles found in tropical regions also have highly varied wing morphology, with a high proportion of species capable of flight and presumably higher vagility (Thiele 1977, Erwin 1985). Although flightlessness may be more common in temperate than tropical regions (Erwin 1979), a high incidence of loss of flight has been observed in high altitude carabid beetle communities in not only temperate North America (Darlington 1943) but also in the tropical Andes (Moret 2009). No matter the latitude, increasing altitude may be associated with a pronounced reduction in resource diversity, primary productivity, and habitat area, and an increasingly unfavorable environment (McCoy 1990). Increased habitat stability and decreased heterogeneity might also favor flightlessness (Kavanaugh 1985; Roff 1990). The present study examines three morphological characters of carabid beetles, body length, wing condition and flight muscle length, along an altitudinal gradient in the cloud forests of the Andes of southeastern Peru. Carabid beetles have only been sampled in the lowland rainforests of Peru and the surrounding Andean region (see Erwin 1991; Moret 2005 and 2009). Furthermore, wing state has been reported for carabid beetles collected in other Neotropical regions, e.g. the Greater Antilles (Darlington 1970) and Ecuador (Moret 2005 and 2009), but not along an altitudinal gradient. Specifically, we will address how body length and flight capability change with altitude within different tribes and for carabid beetle assemblages as a whole. Because of both the increasing environmental homogeneity and abiotic constraints, we predict a decrease in body length and flight capability with increasing altitude. We will also examine differences in these 133 changes along an old growth forest gradient and a disturbed gradient where the forest has experienced anthropogenic disturbance. Because of the relative instability of disturbed habitats, many species of carabid beetles would likely be more vagile, with a higher degree of dispersal ability needed in order to maintain populations. 134 Materials and methods Collections of Carabidae Carabid beetles were collected on two transects, located < 4 km apart in southeastern Peru, K’osñipata Valley (Figure 1). The first gradient is located in the buffer zone of the Manu Biosphere Reserve and follows the Cusco-Pilcopata highway. Extending from 3450 m to 1400 m, the first gradient was sampled at approx. 500 m intervals at five sites in the cloud forest zone, with two additional lowland collection sites at 500 m and 800 m in order to analyze the complete altitudinal gradient. Although the Cusco-Pilcopata highway was finalized in the 1960s (Young and León 1996), a road has existed in the K’osñipata Valley since at least the late 19th century. Since then the areas adjacent to the road have experienced disturbance associated with vehicular traffic, minor agricultural efforts, and timber extraction; we have designated this gradient as disturbed forest. The second gradient, located within the protected area of Manu National Park, follows an Incan trail, the Trocha Union. Extending from 3650 m to 1850 m, the old growth gradient was sampled at approx. 250 m intervals at nine sites, which had already been established by the Andes Biodiversity and Ecosystem Research Group (ABERG). Since this forest has not been logged or cleared (as compared to the disturbed gradient), we have designated it as old growth gradient. Collections on the old growth gradient were made in the mature forest, while the disturbed forest collections were made alongside the road where early succession stage plants, such as grasses and Cecropia, occur sporadically in this area, and mature forest may be 5 -10 m from the road’s edge. Table A1 (Appendix) describes collection sites for both gradients. Due to the limitations of our study, sampling was only replicated by two altitudinal gradients (old growth and disturbed). 135 At each site, carabid beetles were collected by hand, which consisted of sifting through leaf litter on the forest floor and examining above ground vegetation to approximately 1.5 m in height. Hand collections sample only epigeic, i.e. surface dwelling, carabids and possibly exhibit bias based on size of beetle or sampling location. Due to the nocturnal behavior of most carabid beetles, hand collections were conducted at night. Hand collections are preferred to pitfall traps in the tropics as the latter often have a lower yield of abundance and diversity (see Maveety et al. 2011). Search effort was recorded for each site (see Table A3, Appendix). For the disturbed gradient, monthly collections were made from September 2007 to July 2008, with additional collections during December 2008, June 2010 and June 2011. Collections on the old growth gradient were completed during June-July 2010 and May-August 2011. Since there are no taxonomic keys of carabid beetles of the tropical montane forests of Peru, specimens were identified to morphospecies based on external morphology, i.e. without distinguishing between sexes, which has proven to be a useful approach for species inventories (Oliver and Beattie 1996). Specimens were preserved in 95% ethanol upon collection and are currently on loan to the National Museum of Natural History of the Smithsonian Institution, Washington, D.C. Body length A random sample of individuals was measured for each morphospecies, with n = 5 for the 2010 and 2011 collections, and n = 10 for 2007-08 collections. When morphospecies spanned more than one altitudinal zone, at least one individual was measured per zone (see Supporting Information Table S1 for number of individuals). For some morphospecies sample size was limited to the number of individuals collected. Two body 136 length measurements were recorded: Apparent Body Length (ABL) and Standard Body Length (SBL). ABL is the length from the extreme anterior part of the mandible to the extreme posterior part of the abdominal terga or elytra (Cieglar 2000). This is the most commonly accepted measurement for ecological studies (Erwin & Kavanaugh 1981). Because specimens vary in size depending on collection and preservation, SBL measurements were also made. SBL is the sum of three fixed measurements of the dorsal cuticle: SBL 1 = length of head, SBL 2 = length of pronotum, and SBL 3 = length of elytra. Flight condition Wing state was determined by lifting the elytra of a specimen and examining whether a wing was present and, if present, in what state. Wing structure is generally classified as: i) macropterous: alate, or fully winged, ii) brachypterous: reduced wings, and iii) micropterous: wings reduced to stumps or not present (following, e.g. Darlington 1936, Gutiérrez and Menendez 1997). Table 1 lists the description of possible wing states, and images of brachypterous and micropterous wing states can be found in Plates 1-3 of Appendix. Because both brachypterous and micropterous individuals are not capable of flight, i.e. flightless, both groups are referred to as “brachypterous” (see also Kavanaugh 1985). In addition to wing state, flight condition was evaluated by measuring the flight muscle, which attaches to the metasternum and is reduced along the length of the median longitudinal suture in brachypterous specimens (Forsythe 1987). The cuticular medial length of the metasternum (MS) was measured as a proxy for wing muscle and adjusted to account for size differences of carabid specimens using a ratio to ABL (MS:ABL). 137 Flight muscle measurements were made for the same subset of individuals as for body length analyses. Some species were di- or poly-morphic for wing state. For all wing state analyses, di- and polymorphic species were not included. For flight muscle analyses, however, di- and poly-morphic specimens were included. Data analysis ABL was examined both seasonally (rainy and dry seasons, 2007-08 collections) and inter-annually (2007-08, 2010, 2011 collections) in order to detect any differences observed in body length between seasons and among years. For seasonal comparison of body length, data were based on individuals from the 2007-08 collections, which included samples collected in both the rainy season (November to April) and dry season (May to October) (detailed description of seasons can be found in Rapp & Silman 2012). Seasonal and inter-annual differences were compared via single factor, completely randomized design ANOVA, but if variances were heterogeneous (as determined by Fmax test) the Games-Howell Test (Sokal & Rohlf 1995) was used. Body length and flight ability (length of flight muscle and percentage brachyptery) were examined on the altitudinal gradient by regression, for each tribe that spanned three or more altitudinal zones. In addition, regression was conducted for combined carabid beetle assemblages based on all individuals measured for each species at each altitudinal zone. Altitudinal trends in flight muscle were also analyzed independent of wing state (i.e., macropterous or brachypterous individuals) for each tribe that spanned three or more altitudinal zones (by regression), and for the carabid beetle assemblage as a whole. 138 Carabid beetle morphological changes were also compared between the disturbed and old growth gradient. For this analysis the length of the disturbed gradient was truncated at 2000 m to match the altitudinal span of the old growth gradient (1850 m to 3650 m). Group comparison t-tests (assuming unequal variances) were run to compare differences in mean ABL and MS:ABL for tribes that occurred on both the disturbed and old growth gradients. To avoid type I error associated with calculating multiple inference tests, the alpha value is often adjusted by the Bonferroni correction (Sokal & Rohlf 1995). However, as suggested by Moran (2003), the Bonferroni correction increases the chances of committing a Type II error, especially for ecological studies, so alpha was standardized at 0.05. All data analyses were performed in Microsoft Excel. 139 Results Body length A total of 914 carabid beetles were measured, representing 149 total species. Apparent body length (ABL) was a proxy for the sum of the three standard body length measures (ΣSBL). There was a significant positive correlation (r = 0.97, d.f. = 912, F = 1.3*104, P < 0.0001) between ABL and ΣSBL. Based on these data the SBL was approximately 82.8% of ABL. ABL for the entire data set was 7.41 ± 0.22 mm (95% CI), and the length range was 1.94 mm to 23.64 mm. There was no significant difference in ABL among the three different years of collection (Games-Howell comparison, P > 0.05). For 2007-2008 collections, ABL was larger during the dry (7.49 ± 0.072 mm) as compared to the rainy season (7.09 ± 0.096 mm, Games-Howell comparison, P < 0.05). Since no seasonal or inter-annual differences were found, we used data from all months and years in the following altitudinal and disturbed versus old growth comparisons analyses. Nineteen tribes were sampled and ten spanned at least 3 altitudinal zones, qualifying for regression analysis for ABL versus altitude (Figure 2); the tribes presented are monophyletic (T.L.Erwin, pers. comm.). Six tribes (Bembidiini, Clivinini, Galeritini, insertae sedis, Lebiini, and Pterostichini) did not show a significant trend between ABL and altitude. For three tribes (Harpalini, Platynini, and Lachnophorini) the relationship between ABL and altitude was negative, but the ABL-altitude relationship was positive for Trechini. When tribes were divided by subfamily, there was still no singular pattern. When the carabid assemblage as a whole is examined, ABL was negatively correlated with altitude (Figure 2). Although the high abundances of Harpalini and Platynini at first 140 appear to be driving the combined taxa trend, there is still a negative relationship between ABL and altitude when these tribes are removed (r = - 0.43, d.f. = 495, F = 115, P < 0.001). Furthermore, when carabid beetle taxa are combined, the body length of beetles found at or below 2000 m (x¯ = 8.93 ± 0.16 C.I.) was significantly larger that upland carabid beetles found from 2250 m to 3650 m (x¯ = 5.65 ± 0.084 C.I., t = 17, P < 0.001). Flight condition Ten species were found to be dimorphic for wing state and 6 species were polymorphic. Among the di-/poly-morphic species, there were 74% more brachypterous individuals than macropterous individuals. Four di-/poly-morphic species were found within only one altitude zone; the remaining 12 species did not show any trend in wing morphology with altitude zone. All 16 di-/poly-morphic species occurred on the disturbed gradient, with 6/16 of species also occurring on the old growth gradient. For each of the 16 di- /poly-morphic species there was no difference in percentage of individuals that were brachypterous between gradients, except for Dyscolus F, which had more brachypterous individuals on the disturbed gradient (G = 4.09, P < 0.05). For all 16 di-/poly-morphic morphospecies combined there was 71% brachyptery among individuals found along the disturbed gradient and 90% brachyptery among individuals found on the old growth gradient. A total of 133 morphospecies were monomorphic; significantly more species were macropterous (S = 78) than brachypterous (S = 55, G = 4.0, P < 0.05). Flight muscle length was highly variable with altitude among the 10 tribes that spanned at least 3 altitudinal zones (Figure 3). MS:ABL of three tribes (Bembidiini, Harpalini, and Platynini) was negatively correlated with altitude while Lachnophorini was positively correlated. Six tribes did not exhibit a trend in MS:ABL with altitude 141 (Clivinini, Galeritini, insertae sedis, Lebiini, Pterostichini, and Trechini). When tribes were divided by subfamily, there was still no singular pattern. For combined carabid beetle assemblages, flight muscle length decreased significantly with altitude (Figure 3). Although the high abundances of Bembidiini, Harpalini, and Platynini also appear to be driving the combined taxa trend of a negative relationship between flight muscle length and altitude, there is still a negative relationship when those tribes are removed (r = - 0.49, d.f. = 324, F = 104, P < 0.001). Furthermore, when the carabid beetle taxa are combined, the flight muscle of beetles found at or below 2000 m (x¯ = 0.16 ± 0.0014 C.I.) was significantly larger that upland carabid beetles found from 2250 m to 3650 m (x¯ = 0.13 ± 0.0016 C.I., t = 15, P < 0.001). Tribal information about per cent brachyptery is reported in Figure 4; insertae sedis was excluded because it was represented by one dimorphic species, Andinodontis maveetyae. Clivinini and Lebiini were always macropterous, while Galeritini and Trechini were always brachypterous. Otherwise, only one tribe, Bembidiini showed a significant increase in per cent brachyptery on the altitudinal gradient, while the remaining four tribes showed no trend. Per cent brachyptery for the carabid beetle assemblage significantly increased with altitude (Figure 4). Flight muscle was also examined within each wing state class, i.e. macropterous and brachypterous. For macropterous specimens, Lachnophorini and Pterostichini were significantly positively correlated with altitude while Platynini was significantly negatively correlated with altitude (Table 2). For combined taxa there was no trend for macropterous flight muscle with altitude. For brachypterous specimens, Harpalini 142 demonstrated a negative trend, and Pterostichini a negative trend, of MS:ABL with altitude, and the combined brachypterous assemblage demonstrated a negative correlation. Wing state was also examined in relation to body length. To maintain maximum statistical power, individuals were divided into only two groups based on body length: “small” (< 7 mm, x¯ = 5.12 ± 0.14 mm 95% C. I.) and “large” (> 7 mm, x¯ = 11.52 ± 0.48 mm 95% C. I.). For “small” beetles there was no significant difference between number of macropterous species (Sm = 31) and brachypterous species (Sb = 35) (G = 0.24, P > 0.05). In contrast, for “large” beetles there were twice as many macropterous species than brachypterous species (Sm = 49 and Sb = 24; G = 8.74, P < 0.01). This trend was reinforced by a greater MS:ABL length in the large (0.156 ± 0.0034) size group as compared to small (0.131 ± 0.0035) size group (t = 5.0, P < 0.0001). Transect comparison Seven of the 19 tribes were found on both gradients. Since insertae sedis had only one individual on the old growth gradient, only six of the seven tribes could be used for transect analysis. Harpalini, Lebiini, and Platynini had significantly larger ABLs on the disturbed than the old growth gradient while the remaining three tribes were not significant (Table 3). When the entire carabid assemblage was examined, ABL was significantly greater on the disturbed gradient. Only one tribe, Bembidiini, demonstrated a significant difference in length of the flight muscle (MS:ABL) between the two gradients, which was reduced on the old growth gradient (Table 3). Flight muscle was also significantly reduced on the old growth gradient for the entire carabid assemblage. 143 Discussion At the family level, the carabid beetle assemblage demonstrated a decrease in both body length and flight capability with increasing altitude. In contrast, Palearctic carabid species have demonstrated a negative relationship between size and dispersal ability (Loveï & Sunderland 1996). At the finer grained classification level represented by tribes, we observed all possible outcomes between carabid beetle size and dispersal ability with altitude (i.e., positive, negative and no relationship between body length and flight capability with altitude). When comparing disturbed and old growth forests, carabid beetles demonstrated increased dispersal ability and size on a disturbed gradient. Body length The relationship between body length and altitude varied by tribe, with all possible relationships found: positive, negative and no relationship. This suggests that variation in life history strategies may influence how carabid tribes respond to altitude. Decreased temperatures during development, such as that seen on an altitudinal gradient, are thought to limit insect body size (Mousseau 1997), which may be responsible for the negative trend observed in some tribes. However, behavioral adaptations that compensate for cold temperatures, such as burrowing (Sømme et al. 1996), typical of tribes Clivinini and Trechini, might explain both positive and no relationship between altitude and body length. At the family level, a negative relationship between altitude and insect body length was found for carabid beetle species assemblages; we predicted a negative relationship in body length because of four potential constraints on an altitudinal gradient: decrease in resource diversity, reduced habitat area, increase in unfavorable 144 environment, and decrease in primary productivity at high altitudes (McCoy 1990). Decrease in resource diversity could limit body size because of limited energy availability (Chown & Klok 2003). Reduced habitat area may confine organisms with limited vagility to a small area, which could limit body length. An unfavorable environment, such as those as found with decreased temperature and partial pressure of respiratory gases associated with increasing altitude (Hodkinson 2005), could limit body size during development (Mousseau 1997). Finally, a reduction in primary productivity at higher altitudes could effect on the size of carabid beetles if food scarcity and/or habitat scarcity inhibit growth. Andersen (1988) suggested that larger carabid beetles in a community in Norway are associated with larger prey items. Since Neotropical carabid beetles of the high altitude Andes are mostly predaceous with some seed feeders (Moret 2005), primary productivity could have a direct and/or indirect effect. Finally, there could be a thermal component to the negative correlation. Bergmann's Rule which predicts larger sized homeothermic animals in colder environments due to decreased heat loss, but ectotherms may follow the inverse pattern due to increased metabolic rates of smaller organisms (Shelomi 2012). However, it is most likely that the negative assemblage wide relationship between altitude and body length was observed due to the a) variation in altitudinal patterns among tribes and b) change in representation of tribes in both abundance and composition along the altitudinal gradient. Although we outlined trends for ten tribes that spanned ≥ 3 altitude zones, the remaining tribes that spanned ≤ 2 altitudinal zones were exclusively represented by rare species. The trend seen in the assemblage wide ABL also reflects primarily those tribes with high abundance of individuals. Furthermore, carabid 145 beetles were found to have high turnover in species composition along the altitudinal gradient (Chapter III / Maveety et al. in press). For the Harpalini, for example, three relatively large-sized genera, Arthrostictus, Notiobia, and Selanophorus, with an average body length of 10 mm, were encountered from 500 m to 2000 m. They are replaced by a genus with smaller-sized adults, Pelmatellus, with an average body length of 6 mm, at 1400 m to 3650 m. Within each size group, there was no correlation with altitude, supporting the idea that species replacement on the altitudinal gradient may be driving body length trends. Flight condition Darlington (1936) suggested that degeneration of flight muscle might be a secondary result of loss of flight, following the atrophy of wings. Trends found within tribes generally supported loss of flight where brachyptery and flight muscle length are correlated, although the pattern was variable among tribes. Interestingly, Bembidiini, which exhibited a negative correlation between altitude and flight muscle, also showed increased brachyptery with increasing altitude. In contrast, tribes that were represented by only one wing state, either completely macropterous (Lebiini) or brachypterous (Galeritini, Trechini) had no change in flight muscle length across the altitudinal gradient. The higher proportion of brachypterous beetle species at high altitudes (Harrison 1980) may be due partly to the decreased temperature and changes in the physical properties of air, i.e., increasingly thinner air becomes problematic for the generation of lift (Altshuler et al. 2004, Dillon et al. 2006), which makes flight more costly. Loss of flight, however, is not the only solution for an increasingly harsh abiotic environment. For example, hummingbirds have shown increased wing size to compensate for 146 aerodynamic demands on a Neotropical altitudinal gradient (Altshuler et al. 2004). In future studies, it would be useful to examine if wing length of macropterous beetles also change along an altitudinal gradient. We suggest two hypotheses (which are not mutually exclusive) that may explain the increase in incidence of flightlessness observed with increasing altitude: potential for dispersal and energetic constraints. Since dispersal can be important for acquiring food and finding a mate (Kavanaugh 1985; Zera & Denno 1997), selection may favor flight when there is high habitat heterogeneity and more complex habitat dimensionality. Most carabid species are capable of flight in tropical lowlands (Kavanaugh 1985), which are often patchy (Roff 1990; Brehm et al. 2003). However, as altitude increases, environments become increasingly homogeneous (Darlington 1970; Noonan 1985; Roff 1990). Furthermore, habitat stability and persistence are also thought to increase, with both factors favoring selection for flightlessness (Darlington 1943; Kavanaugh 1985; Roff 1990). In addition, if stochastic disasters are reduced for uniform and continuous habitats, flight will not necessarily be advantageous and flightlessness might be adaptive in those areas (Darlington 1936; den Boer et al. 1980). The loss of flight is often prevalent among species inhabiting historically stable habitats where a high degree of dispersal is presumably not necessary such as montane habitats (Wagner & Liebherr 1992; Gutiérrez & Menéndez 1997). For example, in a dimorphic north temperate carabid beetle, Pterostichus melanarius, brachypterous wing morphs are more common in populations occupying more stable habitats (Niemelä & Spence 1991). Furthermore, planthoppers (Delphacidae) (Denno et al. 1991) have shown decreased macroptery in more persistent habitats as related to altitude. The high population densities often found 147 at high altitude (Hodkinson 2005) places beetles in close proximity to one another and flight may not be the most efficient means of finding a mate. A second hypothesis for increased brachyptery at higher altitudes focuses on the trade-off between the energy required for development of morphological flight apparatus versus the increased energetic costs associated with high altitudes (Hodkinson 2005). The cost of flight apparatus may outweigh the cost to reproduce and survive at high altitude because of the energetic limitation of the high altitude habitat (Mani 1968; Ikeda et al. 2012). The wings of an insect can be energetically expensive, constituting 10% to 20% of the total body mass (Roff 1990). If energy resources are scarce and/or energy is expended more rapidly in the colder temperatures that occur at high altitudes there could be a trade- off between expending energy on wing development and flight versus energy needed for survival, growth and reproduction (Erwin 1979, Hodkinson 2005). Transect comparison A reduction in body size of carabid beetles has often been reported for disturbed areas (Blake et al. 1994; Raino & Niemelä 2003; Ribera et al. 2001; Jelaska & Durbešić 2009). Niemelä et al. (2000) suggest that there should be a negative correlation between carabid beetle size and degree of disturbance due to the increased survival rate of smaller beetles in disturbed areas. However, in our study, there was variability in body length among tribes but the carabid beetle assemblage as a whole exhibited larger body lengths on the disturbed gradient; these results do not support Niemelä et al. (2000), and could likely be due to low statistical power. Dung beetles in Indonesia, on the other hand, also had increasing body length with greater levels of disturbance (Shahabuddin et al. 2010). Schoener and Janzen (1968) suggest that larger insects are more desiccation tolerant. If so, 148 dry habitats, such as disturbed habitats, may support larger species. It is important to note, however, that body length (which was measured in this study) does not necessarily correlate with body size, although that is usually the case. Insects with larger mass, not necessarily longer insects, might be more drought tolerant. Alternately, body length may vary because of the change in species between the two gradients that could be linked to changes in food sources (Lövei & Sunderland 1996). In general, flight muscle length did not change for tribes that occurred on both gradients. Although some tribes were either completely macropterous or brachypterous, the remaining tribes exhibited a greater per cent brachyptery on the old growth gradient, even though it was non-significant. Increased macroptery has been reported for disturbed habitats (e.g. Ribera et al. 2001) and was expected due to the need for increased dispersal ability to find more suitable habitats (Thiele 1977). 149 Conclusions The results from this study indicate that for an Andean elevation gradient the relationship between altitude and wing state is complex, with the results depending upon which tribes are examined and whether the forest on that gradient has been disturbed. Body length and incidence of flightlessness were highly variable, when examined by tribe, along the altitudinal gradient, which could be affected by the more limited number individuals once the data were divided among tribes. Furthermore, results differed from trends commonly reported for Palearctic carabid beetles, e.g., larger bodied carabid beetles were more likely to have increased dispersal in our study. Future studies should take into account not only taxa variability but also habitat heterogeneity and disturbance. More exhaustive sampling, as well as increased replications of transects and altitude zones would decrease the potential for sampling error. 150 Acknowledgements Financial support was provided by the Fulbright Program, National Museum of Natural History at the Smithsonian Institution, the Entomological Society of America, and Wake Forest University. Collection and export permits were obtained from the Peruvian Ministry of Agriculture, Instituto de Recursos Naturales, and Servicio Nacional de Áreas Naturales Protegidas por el Estado, with the help of the Entomology Department at the Museo de Historia Natural de la Universidad Nacional Mayor de San Marcos. We thank the Amazon Conservation Association (ACCA), PeruVerde, and ProNaturaleza for logistical support. A special thanks to W.E. Conner, Wake Forest University, for useful comments of an earlier version of the manuscript, and to T.L. 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Flight muscle (MS:ABL) correlation with altitude between Macropterous and Brachypterous individuals for tribes that span at least three altitudinal zones. “N/a” indicates that a tribe had no individuals designated for either of the two wing state groups. Macropterous Brachypterous Tribe r F P r F P Bembidiini 0.062 0.13 0.72 - 0.055 0.40 0.53 Clivinini 0.30 2.7 0.11 n/a Galeritini n/a - 0.064 0.087 0.77 Harpalini - 0.12 2.7 0.10 - 0.26 4.0 0.050 Insertae sedis n/a - 0.10 0.077 0.79 Lachnophorini 0.36 11 0.0013 n/a Lebiini 0.30 2.3 0.15 n/a Platynini - 0.48 23 < 0.001 0.087 0.59 0.44 Pterostichini 0.60 7.9 0.014 0.96 22 0.042 Trechini n/a - 0.072 0.51 0.48 All Individuals - 0.052 0.34 0.56 - 0.30 13 < 0.001 161 162 List of Figures Figure V - 1. Map of study area and location of collection sites. Figure V - 2. Altitudinal trends in apparent body length (ABL) of carabid beetles for tribes that span at least three altitudinal zones. The bottom right panel represents ABL (x¯ ± CI) for all 19 tribes, with regression based on all individuals at each altitudinal zone. A solid trend line indicates a significant correlation, and a dotted trend line indicates no significant correlation. Note variation of y-axis, body length, among panels. Figure V - 3. Altitudinal trends in flight muscle length (MS:ABL) of carabid beetles for tribes that span at least three altitudinal zones. The bottom right panel represents MS:ABL (x¯ ± CI), for all 19 tribes, with regression based on all individuals at each altitudinal zone. A solid trend line indicates a significant correlation, and a dotted trend line indicates no significant correlation. Figure V - 4. Altitudinal trends in per cent brachyptery by tribe. The bottom panel represents total per cent flightless species from all 19 tribes. A solid trend line indicates a significant correlation, and dotted or no trend line indicates no significant correlation. 163 Figure V – 1 164 Figure V – 2 165 Figure V – 3 166 Figure V – 4 167 CHAPTER VI CARABID BEETLE ASSEMBLAGES (COLEOPTERA: CARABIDAE) ON ANDEAN AND APPALACHIAN ALTITUDINAL GRADIENTS The following manuscript will be submitted to Environmental Entomology (12/2013). Stylistic variations are due to the requirements of the journal. 168 Abstract Species richness, community composition and morphological characters of carabid beetles (Coleoptera: Carabidae) are compared between a tropical gradient in the Peruvian Andes and a temperate gradient in the southern Appalachian uplands. Carabid beetles were collected for one year in southeastern Peru at five altitudinal zones ranging from 1400 m to 3450 m. Carabid beetles were also collected for one year on a transect in the Great Smoky Mountains National Park (GSMNP), with pitfall traps established at six altitudinal zones ranging from 600 m to 2000 m. The Andes had higher species richness than the Appalachians with both gradients demonstrating middle altitude peaks in species richness; there was only a significant curvilinear correlation of richness with altitude for Appalachian assemblages, although the middle altitude peak in richness in Andean assemblages was significantly greater than adjacent altitudes. Species assemblages between the two gradients were compositionally distinct, with the carabid beetle assemblage of the Andes more even than the Appalachian assemblage. For both the Andes and Appalachians, species assemblages differed significantly between adjacent altitudinal zones, with species turnover rates varying by altitude. On average, carabid beetle body length was 66% longer in the Appalachians, with body length negatively correlated with increasing altitude for both gradients. The proportion of flightless species was also positively correlated with increasing altitude in the Andes, but not in the Appalachians, where more than 90% of the species are flightless at all elevations. Keywords: body size, dispersal ability, Great Smoky Mountains National Park, Peru, species richness 169 Introduction The question of how organisms are distributed along altitudinal gradients in tropical and temperate montane forests has been of long standing interest (e.g., Humboldt and Bonpland 1807; Darlington 1943; Whittaker 1956). While some studies have reported a decline in species richness with increasing altitude (e.g., birds, Terborgh 1977; trees, Gentry 1988; insects, Hanski and Niemelä 1990, and Hodkinson 2005), other studies have reported a middle altitude peak (e.g., Lepidoptera, Brehm et al. 2003 and non-volant mammals, McCain 2004). Complicating the search for a common pattern is that both trends have been reported for both tropical and temperate regions of the world. The eastern slopes of the Andes Mountains in Peru extend from the lowland tropical rainforest of the Amazon Basin at about 250 m to extreme alpine conditions above 4000 m. Specialized atmospheric conditions of relatively cool temperatures and high humidity produce cloud-shrouded forests within a portion of that gradient, extending from approximately 1500 m to 3500 m, at or near timberline (Young and León 1999). The tropical montane forests of the eastern slopes of Peru harbor among the world’s highest biodiversity and endemism (Myers et al. 2000; Feeley and Silman 2010), but are threatened by settlers, loggers, and conversion to agriculture (Young and León 1999). Cloud forests may also be important in the context of climate change. As global temperatures increase, clouds are expected to form at higher altitudes, and zonal climate shifts could affect numerous taxa, potentially leading to species extinctions (Pounds et al. 1999; Nadkarni and Solano 2002; Williams et al. 2007). The Great Smoky Mountains National Park (GSMNP), in the southern Appalachian Mountains, USA, also has high moisture and cloud cover creating an 170 environment similar to the eastern Andean slope. Although generally less species rich than the tropics, GSMNP has among the highest levels of biodiversity in the temperate zone for a variety of taxa, e.g., trees (Shanks 1954), salamanders (Petranka et al. 1993), and bryophytes and lichens (White et al. 1993). Fragmentation of the spruce-fir forests in the southern Appalachians, following a gradual climate warming trend after the Pleistocene, created “sky islands” that serve as habitat for many species not found elsewhere in the southeastern United States (Whittaker 1956; White et al. 1993; Crespi et al. 2003). The southern Appalachians, especially the spruce-fir ecosystems, also face the impending threat of climate change (White et al. 1993). Both regions support exceptionally high levels of diversity and endemism for their respective ecosystems (e.g., Carlton and Bayless 2007; Stotz et al. 1996). Previous studies have suggested that carabid beetles (Coleopetera: Carabidae) are useful biological indicators for forest ecosystems (e.g., Niemelä et al. 2000; Rainio and Niemelä 2003). They not only successfully signal environmental and ecological change (Niemelä et al. 2000), but also vary widely in physical attributes, taxonomy, behavior and ecology (Erwin 1979). They are collected relatively easily, and their preparation, description, and identification for analysis are relatively uncomplicated (Lövei and Sunderland 1996). Although most carabid beetle studies (e.g., Greenslade 1964; Gutiérrez and Menéndez 1997, Ortiz and Browne 2011, Browne et al., submitted) utilized pitfall trapping due to the high number of individuals captured per unit of effort and the robustness of the statistical analysis, such studies were conducted in the temperate region. For carabid beetle sampling in the Andes, hand collections have a higher yield of species for a fixed number of individuals sampled than pitfall traps (Chapter II / Maveety et al. 171 2011). While using the same sampling technique for comparison of Andean and Appalachian beetle assemblages would at first glance appear to be a more direct comparison, we believe the preferred approach is to use the sampling techniques that yield the highest number of individuals and most diverse sample set for each region. Studies on altitudinal gradients have a bias towards the tropics, probably due to the higher climatic variation that occurs on a tropical altitudinal cline (Rahbek 1995). However, most studies on carabid beetles tend to come from the temperate region (Rainio and Niemelä 2003). In general, tropical diversity is expected to be higher than that of temperate regions (Mittelbach 2007), e.g., for vascular plants species richness is an order of magnitude greater in the tropics (Gentry 1988). However, few studies have been conducted to actually compare the relationships between altitude and species diversity for temperate versus tropical regions (but see Jankowski et al. 2009). In order to partially address this gap, we compare carabid beetle assemblages sampled from transects in montane cloud forests of the Andes and the Appalachian mountains. We predict compositionally distinct assemblages between the two regions, with greater diversity in the tropical region. Because of the increasingly harsh abiotic environment reported for altitudinal gradients, (e.g., Hodkinson 2005), we also predict a decrease in species richness as altitude increases, regardless of region (see also Maveety et al. 2011). In addition, we examine differences in two morphological characters, body length and wing condition, in relation to altitude. Carabid beetles have shown decreased body length and dispersal ability along a Neotropical altitudinal gradient (Maveety and Browne submitted / Chapter V); an increasingly restrictive abiotic environment will likely influence these morphological characters for both regions. 172 Materials and Methods Data collection Appalachian Mountains. A transect was established on Clingmans Dome (Tennessee- North Carolina border), the highest point in GSMNP and among the highest peaks in eastern North America (Fig. 1a). Six sampling stations were established 50 -100 m adjacent to the highway at approximately 200 m altitude intervals, ranging from 675 m to 1975 m. Appendix Table A2 lists the altitude and GPS coordinates for each site. Each pitfall trap was constructed by embedding a 16-ounce plastic cup in the soil with the rim flush with the ground. In order to account for possible microsite variation, at each sample site two clusters of traps were placed at least 10 meters apart, with six traps per cluster for a total of 12 traps per site. Cups were filled halfway with propylene glycol, which kills and preserves arthropods and is non-toxic for mammals. A flexible foam cover (12 x 12 cm), raised approximately 1 cm above each cup (via nails partially pushed into the soil) prevented excess rainwater and debris from entering the cup. Each month, the contents of each cup were drained and passed through a fine mesh strainer. Collections occurred monthly from June 2006 through May 2007. Adult carabid beetles were preserved in 95% ethanol and transported to Wake Forest University where they were sorted to species level and stored. Species identifications were made primarily based on a key to the carabid beetles of South Carolina by Cieglar (2000). Andes Mountains. Carabid beetles were collected at sites adjacent to the Cusco-Pilcopata highway in the Cultural Zone of Manu National Park, Department of Cusco, Peru (Fig. 1b). Five sampling sites were established; each was located at the forest edge along the road, at approximately 500 m altitudinal intervals extending from 1400 m to 3450 m (see 173 Appendix Table A1 for GPS and altitude data). At each site, carabid beetles were collected via hand searches, which consisted of sifting through leaf litter along the forest floor and examining above ground vegetation to approximately 1.5 m in height. Due to the nocturnal behavior of most carabids, hand collections were done at night. Sampling was conducted from September 2007 to July 2008 and December 2008 (see also Maveety et al. 2011). In order to provide an estimate of search effort, the number of collectors and search time were recorded for each site (see Appendix Table A3). Since neither a specific key to high altitude Andean carabid beetles nor a list of species for this area was available, specimens were sorted to morphospecies, based on external physical attributes recognized and utilized by workers in carabid taxonomy. It is important to note that both hand (Andes sites) and pitfall (Appalachian sites) collection techniques sample only the epigeic, or ground dwelling assemblage of carabid beetles. Species richness and community composition Since sampling effort varied among altitudinal zones and between regions, species richness was interpolated, or rarified, using the Mao Tau richness estimator (EstimateS Version 9, Colwell 2013). Extrapolated estimates of species diversity, asymptote of S for the observed assemblage, were measured using the non-parametric Chao 2 estimator from EstimateS (Gotelli and Ellison 2013). The difference between means of richness estimators was compared using p-values calculated in R 2.13.1 (Shannon-Wiener, Fisher’s alpha), community indices (Shannon’s evenness, probability of interspecific encounter, and Sørensen’s similarity index), and dominance (Berger- Parker index) were calculated (see Magurran 2004 for description of the various 174 estimators). Two sample t-tests (assuming unequal variances) were used to examine assemblage wide differences between Andean and Appalachian data sets, with altitude as a replicate, and general regression models were run on rarified species richness and community metrics versus altitude, all calculated in Microsoft Excel. Community composition was evaluated via non-metric multidimensional scaling (NMDS) using PCOrd Version 4 Curtis) index was used as the distance measure, and NMDS was calculated with the “slow and thorough” autopilot mode option, which chooses the best solution starting from six axes (from 400 iterations, 40 runs with real data and 50 randomized runs) (McCune et al. 2002). Morphological comparisons Body length. Body length for each specimen was measured as apparent body length (ABL) to the nearest hundredth of a millimeter, as described by Cieglar (2000). ABL measures from the anterior most part of the mandible to the posterior most part of the individual’s body, and is the most commonly accepted measurement of body length for ecological studies (Erwin and Kavanaugh 1981, see Chapter V). For Andean collections, ABL for each specimen was recorded at the time of morphospecies sorting (see Appendix Table A5). For Appalachian collections, ABL was estimated for each species based on values published in Cieglar (2000) using the midpoint of the stated species size range. To verify ABL methods of the Appalachian collections, measurements were compared to average sizes recorded by Chavez (2006) for GSMNP sites; in that study 59% of the beetle species for which length measurements were reported were also collected in the present study. While the values for Appalachian species may be less accurate than those 175 for the Andes, we believe they are sufficient for inter-regional comparisons. ABL values reported from both studies were highly positively correlated (y = 0.88x + 2.07, r = 0.94, d.f. = 18, F = 134, P < 0.0001). Pitfall traps may be biased toward larger, more mobile species (Greenslade 1964); hand collections may also represent larger species since they are easier to see at night with headlamps. Smaller species are probably underrepresented in both Andean and Appalachian data sets. Wing condition. For Appalachian collections, wing state for each species was based on wing-characterizations provided in Larochelle and Larievière (2003). Because most Andean carabid beetles species are not described, wing state was determined based on anatomical examination of all individuals from each species. Wing states were grouped as either capable of flight (i.e., fully developed wing) or flightless (i.e., vestigial wing or wing pad); see Chapter V for a more detailed description of wing states. 176 Results Species richness and community composition A total of 3563 individuals representing 34 species were collected over one year in the southern Appalachians; in the Andes, 1556 individuals, representing 66 species, were collected over one year. A comparison of species accumulation curves for Appalachian and Andean collections (Fig. 2) indicates that the carabid beetle assemblage in the Appalachian region was more completely sampled and less species rich. When species number was rarified (Sr based on Mao Tau richness estimator) at n = 1556, the Andean collection was more than twice as species rich as the Appalachian collection (Sr = 66 ± 5.0 and Sr = 27 ± 2.3, respectively, P < 0.0001). The Appalachian curve approached asymptote at approximately 34 species while species continue to accumulate at all points of the curve for the Andean data. The Chao 2 richness estimator reported approximately 38 ± 4 (x¯ ± SD) species for Appalachian assemblage and 102 ± 15 species for Andes assemblage (P < 0.0001). Neither gradient showed a significant correlation between raw species number and altitude (rAp = 0.18, rAn = 0.83). However, rarified species richness showed a significant negative curvilinear trend with altitude for the Appalachian gradient (Fig. 3, r = 0.94, P < 0.01), with richness peaking at 1400 m. There was a similar middle altitude peak in Sr for Andean data, although the correlation was not significant (r = 0.77, P > 0.05), possibly because of the limited statistical power based on five data points. There was no difference in the means of Sr between adjacent altitudinal zones for the Appalachian assemblage (0.17 ≤ P ≤ 0.42 for the entire gradient), but for the Andean gradient, 2000 m had a significantly higher Sr than both 1400 m and 2500 m (P < 0.01). 177 Table 1 lists diversity and dominance values for both Andean and Appalachian carabid beetle collections. There was no significant difference between Appalachian and Andean assemblages for any diversity, community, or dominance value, with all P ≥ 0.09 (independent t-test assuming unequal variance). There was also no correlation with altitude for any diversity, community, or dominance values for either region, with all P ≥ 0.07. Although there was variation by elevation, total values for Shannon-Wiener, evenness and dominance were approximately the same for the Andean and Appalachian gradients. Fisher’s alpha, however, was more than 200% higher for the total value on the Andean gradient than the Appalachian gradient, supporting a higher level of species diversity for the entire Andean gradient. For Andean collections, the 2000 m site had the highest diversity, as estimated by Shannon-Wiener (2.58) and Fisher’s Alpha (7.29) while 1400 m had the highest dominance value (0.72). Shannon’s Evenness and PIE were highly variable among the five Andean sites, but exhibited little variability along the Appalachian altitudinal gradient. Sørensen’s similarity index was higher in the Appalachian assemblages (x¯ ± 95% C.I., Andes: 0.39 ± 0.10, and Appalachian: 0.68 ± 0.02), but not significantly (t = 2.82, P = 0.06) (Table 1). There was no correlation between altitude and species turnover for either region. There was a higher degree of specialization for the Andes with 64% of beetle species found in only one altitudinal zone, compared to 26% of beetle species for the Appalachians. No species in the Andes was found on the entire gradient (5 altitudinal zones, 2050 m range), but 15% of the Appalachian species in the Appalachian were found on the entire gradient (6 altitudinal zones; 1300 m range). 178 NMDS analysis for the Appalachian data (Fig. 4a) indicated a clear distinction between lower altitude sites (600 m to 1400 m) and upper altitude sites (1600 m to 2000 m). Axes 1 and 2 represented 54.2% of the variability (axis 1: r2 = 0.264, axis 3: r2 = 0.278), with altitude possibly representing a large component of axis 2. In the southern Appalachians, spruce-fir forests mix with hardwoods at approximately 1600 m and are the dominant trees at higher elevations. In contrast, the Andean sites do not cluster by altitude (Fig. 4b). For Fig. 4b, 51.4% of the variability was explained by axes 1 (r2 = 0.217) and 3 (r2 = 0.297). There was no overlap between species or genera present in the Appalachians and those present in Andes, as expected. Relative abundance curves showed that, in addition to being more diverse, the Andean assemblage is also more even, with more equivalent abundance among species, as compared to the Appalachian assemblage (Fig. 5). There was no trend when examining the rank abundance curves by altitudinal zone (not shown) for either the Appalachians or the Andes. Body length The ranges of body lengths for both regions were similar; 23.6 mm (5.9 mm – 29.5 mm) for the Appalachians and 21.7 mm (1.9 mm – 23.6 mm) for the Andes. However, when averaged over all species and elevations, the mean value of body length for the Appalachians, 14.24 +/- 0.73 mm (x¯ ± 95% C.I.), was 66% larger than the Andean value of 8.56 +/- 0.48 mm (t = 6.42, P < 0.001). Body length of Andean carabid beetles was negatively correlated with altitude (y = -0.0020x + 12.3; r = 0.93, d.f. = 4, F = 19.8, P = 0.02) (Fig. 6). Although the correlation with altitude for Appalachian carabid beetle 179 length was not significant (r = 0.54, P > 0.05), the best-fit slope was similar to that for the Andean data (y = -0.0017x + 18.8, Fig. 6). Wing condition There was no correlation with altitude and percent of flightless species for either the Appalachian or the Andean gradients (Fig. 7). For the Appalachian gradient the proportion of flightless species was greater than 90% at all altitudes. In contrast, for the Andes the percent of flightless species ranged from 9% to 72% among altitudinal zones. There was a significantly smaller proportion of flightless species for the Andes (46% ± 11.1%) than the Appalachians (98% ± 1.18%, t = 4.57, P = 0.01). 180 Discussion Species richness and community composition Darlington (1943) noted that, based on field observations, tropical montane carabid communities differ greatly from their temperate counterparts. The current study supported Darlington’s early observation. At any given altitudinal zone and when all altitudinal sites were integrated into a composite value, Andean carabid fauna had significantly more species than that found in the Appalachians. This finding is supported in other taxa such as vascular plants, in which richness was an order of magnitude greater in tropical forests as compared to temperate forests (Gentry 1988) and birds which were six times more species rich in Latin America than North America (Jankowski et al. 2009). In both regions, however, carabid beetle species richness declined with altitude. A significant curvilinear regression between rarified species richness and altitude in the Appalachian assemblage suggests a middle altitude peak in species richness. There was also a suggestion of an asymmetrical middle altitude peak in richness for the Andean assemblage as the richness of the 2000 m zone was significantly greater than adjacent zones, although the correlation was not significant. The pattern observed for the Andes data may have been affected by whether arboreal species were included in sampling. In the tropical lowlands up to 50% of carabid species may be arboreal (T.L. Erwin, pers. comm.) and increasing altitude presents an increasing proportion of species that are both epigeic and arboreal; diversity of epigeic carabid beetles, those sampled in this study, may peak at middle altitudes where arboreal species begin to drop out. Alternatively, the observed peak at middle altitudes in the Andes assemblage could be an artifact of the 181 truncated altitudinal gradient (at 1400 m); sampling of the complete gradient may be necessary to draw conclusions about altitudinal richness patterns in carabid beetles. The peak in species richness did not occur at the same altitudinal zone for the Andes (2000 m) and Appalachians (1600 m). Although they are both continental ranges, the Andean gradient extends to 3450 m, while the Appalachians gradient range is limited to 2000 m (the mid-altitude richness peak on the Andean gradient). The Massenerhebung effect, i.e., the effect due to a mountain range’s mass (Richards 1996), and the more extreme physical properties of high altitude, such as thinning air and decreasing temperature (Hodkinson 2005), are likely more pronounced on the Andean gradient. Beta diversity was greater between any two adjacent altitudinal zones in the Andean assemblage than in the Appalachian assemblage. Tropical montane species likely have smaller altitudinal ranges than their temperate counterpart (Jankowski et al. 2009), which may contribute to the increased compositional turnover in the Andean assemblage. Andean and Appalachian carabid beetle assemblages were taxonomically distinct, with no overlapping genera. Non-metric multidimensional scaling showed that the composition within the Appalachian assemblage changed with altitude. Appalachian assemblages were divided into a low altitude cluster and a high altitude cluster, which corresponded to lowland forests dominated by hardwood tree communities (600 m to 1400 m), and high altitude spruce-fir forests which dominate above ca. 1400 m (White et al. 1993). It is likely that the structural changes in forests along the Appalachian gradient are influencing carabid beetle assemblages. Andean carabid beetle assemblages were more even than Appalachian assemblages, as demonstrated by rank abundance plots. The Appalachian carabid beetle 182 abundances were similar to the geometric series predicted for temperate forests with low diversity and high dominance (Hubbell 1997); the Andean assemblage, on the other hand, had higher diversity and more even distribution of abundances, as seen in the nearly log- series shape. However, results should be viewed with caution for the Andean assemblage because the entire community is not as completely sampled as the Appalachian assemblage (per species accumulation curves). Body length Physical constraints along an altitudinal gradient affect not only species diversity and community composition but also morphological traits. There was a significant negative correlation between body length and altitude for the Andes but not for the Appalachians. Tropical altitudinal gradients represent a wider range of climatic variation than their temperate counterparts (Rahbek 1995), which may help explain the negative correlation for the Andes. The range of elevations sampled was also larger for the Andes (2050 m) than for the Appalachians (1300 m). The energetic considerations of an organism likely play a large part in the determination of optimal insect size between temperate and tropical regions and at different altitudes. Appalachian carabid beetles had significantly longer body length on average than those from the Andes. However, Schoener and Janzen (1968) predicted the opposite trend, reasoning that insect size would be positively associated with length of growing season. Since temperate regions are limited by a shorter growing season, especially in the higher altitudes of the Appalachian Mountains, smaller body sizes would be expected. However, the longer and presumably larger body sizes found for the Appalachian beetles might be 183 more adaptive for multi-year reproduction (iteroparity) and overwintering, which occurs for many temperate zone carabid species (Thiele 1977; Larochelle and Larivière 2003). Phylogenetic constraints could also at least partially explain the differences in body length between Andean and Appalachian carabid beetle assemblages. Although there was no overlap of genera between the two regions, there were three tribes found in both regions: Harpalini, Pterostichini and Platynini. For each of these three tribes, body length was on average at least 2 mm larger for the Appalachian beetles compared to the Andean counterparts. The beetles collected exclusively from the Andes also contain proportionally more tribes with small-sized species, e.g., Bembidiini and Trechini (Erwin 1979). Likewise, both tribes that were exclusive to the Appalachian assemblage, Licinini and Cychrini, are tribes of mostly large-sized adults, with the latter representing 45% of the individuals and 34% of the species of the Appalachian assemblage. Wing Condition Wing condition of Andean carabid beetles was highly variable with altitude while more than 90% of carabid species were flightless at all altitudes for the Appalachians. For Andean assemblages, less than 30% of the species were flightless at the lowest altitudinal zones (1400 m and 2000 m), which is consistent with Thiele’s (1977) observation that most carabid beetle species are winged in tropical lowlands. More than 30% of tropical carabid fauna are arboreal (Lövei and Sunderland 1996), while the temperate value might be as low as 7% (Erwin 1979). The high proportion of flightless species in the Appalachians indicates that they are principally ground dwellers and are probably poor dispersers; although this finding may be an artifact of the pitfall trap collection technique employed on the Appalachian gradient (Liu et al. 2007). 184 Darwin’s early observation of the high level of brachypterous beetles of Madeira led to his hypothesis that island winds would blow flying insects out to sea and therefore select for increased brachyptery on islands (Darwin 1859, Erwin 1985). Mountain tops are similar to islands due to their isolated nature, and wind speed is thought to increase on an altitudinal gradient (Hodkinson 2005). Although wind speed is slightly higher at lower altitudes in the Andes, it averages about 1 ms-1 across all altitude zones (Rapp and Silman 2012). In contrast, wind speed increases with altitude in the Appalachians, with a mean value of approximately 4 ms-1 at the highest elevations (Petty and Lindberg 1990, AMEC Report 2011). Increased wind speeds may explain why only a very low proportion of Appalachian carabid beetles are capable of flight. Conclusions This comparative analysis should be viewed as preliminary. The differences in collection methods between the Appalachian and Andes may reflect different sampling biases. In the Appalachians, the altitudinal range that was sampled was less than that of the Andes, which may have contributed to the higher species number found in the Andes. Only one transect was employed in both regions, leading to possible sampling error. While recognizing these limitations, we believe that this study, which represents sampling over a one-year period and along extensive elevation gradients, is a beginning step in understanding changes in species diversity and composition on elevation clines in both temperate and tropical region. Future studies, involving multiple transects, multi-annual sampling periods, and multiple locations, will undoubtedly improve our understanding. 185 Acknowledgments We thank T.L. Erwin, C.E. Carlton and V.M. Bayless for expertise with carabid beetle identifications, and Peruvian NGOs, Amazon Conservation Association (ACCA), PeruVerde, and ProNaturaleza and the Entomology Department at the Museo de Historia Natural de la Universidad Nacional Mayor de San Marcos for logistical support. Financial support was provided by the Fulbright Program, National Museum of Natural History at the Smithsonian Institution, and Entomological Society of America, and Wake Forest University. 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Center for Research on the Cultural and Biological Diversity of Andean Rainforests (DIVA), Copenhagen, Denmark. 193 194 List of Figure Headings Figure VI - 1. Map of sampling sites in A) the southern Appalachian Mountains, USA, and B) the Andes Mountains of southeastern Peru. Figure VI - 2. Species accumulation (Mao Tau species richness estimators), based on accumulating number of individuals, for Appalachian and Andean carabid beetle assemblages. Dashed lines represent 95% confidence intervals. Figure VI - 3. Rarified species richness (Mao Tau) by altitude for Appalachian and Andes sites. Bars represent 95% confidence intervals. The line fit is significant for the Appalachian data (P < 0.05) but not for the Andes data. Figure VI - 4. Non-metric multidimensional scaling (Sørensen index) for Appalachian and Andean carabid beetle species assemblages. Figure VI - 5. Relative abundance plots for Appalachian and Andean carabid beetle assemblages. Figure VI - 6. Mean body length of carabid beetles as a function of altitude at Appalachian and Andes sites. Bars represent 95% C.I. The regression line for the Andes data is significant (P < 0.05), but not for the Appalachian data. 195 Figure VI - 7. Percent flightless species by altitude for Appalachian and Andean carabid beetles. 196 Figure VI ‒ 1 197 Figure VI ‒ 2 198 Figure VI ‒ 3 199 Figure VI ‒ 4 200 Figure VI ‒ 5 201 Figure VI ‒ 6 202 Figure VI ‒ 7 203 CHAPTER VII CONCLUSIONS AND FUTURE DIRECTIONS This dissertation project was the first attempt at the collection of Carabidae (Coleoptera) along an altitudinal gradient in the Andes of southeastern Peru and one of the few studies of tropical insects based on relatively large data sets where sampling occurred on more than one gradient with more than one year of data. In Chapter II, I found a significant negative correlation between raw species number and altitude. Most species were rare and restricted to only one altitudinal site and no species was found at more than three of the five altitudinal sites. Only one genus, Pelmatellus (Tribe Harpalini), was found at all five sites (1400 m to 3400 m). Active (hand) collections yielded almost four times as many individuals as passive pitfall traps, and sampled approximately twice as many species. Hand collections sampled a similar assemblage as pitfall traps; most species found in pitfall traps were also found in hand collections; only 8% of total species collected were unique to pitfalls. Multiple collection techniques are often employed for total biodiversity surveys (e.g., see Erwin 1996), but I found that hand collections were more efficient for collections of carabid beetles in the tropics. In Chapter III, species richness, adjusted for sample size, is analyzed by altitude. As proposed by Rahbek (1995) there was a middle altitude peak in rarified species richness. Similarity between species assemblages from adjacent altitudinal sites ranged from 20% to 52%. Species richness was approximately 10% higher in the rainy season than the dry season, with only 64% of species occurring in both seasons. Despite the 204 importance of multi-seasonal survey sampling for Neotropical habitats, most surveys to date have been limited to the dry season. The results of this study highlight the importance of sampling during a complete seasonal year, with periodic collections throughout each season. In Chapter IV, I examined species richness and community assemblages on two altitude gradients: an anthropogenically disturbed gradient and an old growth gradient. I found that there was no significant trend with altitude between the gradients for raw species number, rarified species richness, diversity metrics (Shannon-Weiner, Fisher’s alpha) or community metrics (Shannon’s evenness, probability of interspecific encounter). Both gradients had similarly even species assemblages, but varied markedly by composition (when analyzed using non-metric multidimensional scaling) with an average similarity of 40% between gradients. The 2008 collection year was less species rich than both 2010 and 2011, but there was no compositional difference. In Chapter V, I found that body length and incidence of flight decreased with increasing altitude. However, these patterns were not uniform among tribes. Body length was significantly negatively correlated with altitude for the most abundant tribes, but other tribes had significant positive correlation or no correlation. This was also true for flightlessness: For all carabid beetles combined there was a significantly positive correlation between altitude and percent flightless species and a significantly negative correlation between altitude and length of the flight muscle, but the breakdown by tribe again showed high variability. Carabid beetles had larger body lengths and a higher incidence of flightlessness on the disturbed gradient than the old growth gradient. Carabid body length and dispersal ability along an altitudinal gradient may be influenced 205 by the energetic considerations for an organism living at high altitude. Increasing habitat stability and decreasing heterogeneity of high altitude forests may also affect carabid dispersal ability. As expected for tropical regions, the Andean carabid beetle assemblage had higher species richness than the Appalachian Mountains of North Carolina, with both gradients demonstrating middle altitude peaks in species richness (Chapter VI). Species assemblages between the two gradients were compositionally distinct, with the carabid beetle assemblage of the Andes more heterogeneous than the Appalachian assemblage. Andean assemblages exhibited high variability in compositional similarity between altitudinal zones, ranging from 20% to 63%, while Appalachian assemblages were always highly similar (ranging from 61% to 73%). Average carabid beetle body length was 66% longer in the Appalachians, and body length negatively correlated with increasing altitude for both gradients. The proportion of flightless species was positively correlated with increasing altitude in the Andes, but not in the Appalachians, where more than 90% of the species are flightless at all elevations. Future Research There is probably not one simple explanation for patterns of species diversity found along altitudinal gradients (Rahbek 1997). Extensive sampling over multiple years and for additional transects would greatly increase our understanding of how carabid species assemblages change with altitude, season, and annually. Nevertheless, this study is the first systematic sampling of carabid beetles over multi-year cycle and at multiple elevations of a tropical montane forest. The results indicate that tropical montane species 206 assemblages change significantly with altitude and season, but not by year. Additional studies are needed to document the full extent of these changes, which could be especially relevant in light of the potential effects of climate change Tropical arthropod inventories are methodologically challenging for diversity estimates (Brehm et al. 2003). Based on my research, I would suggest enhanced sampling regimes for future studies of carabid beetles in the tropics. In order to obtain a better picture of the Andean carabid beetle fauna, additional collection techniques must be employed. Pitfall traps and hand collections sample the epigeic, or ground dwelling community of carabid beetles. However, carabid beetles occupy a variety of habitats in the tropics: arboreal species could be sampled by arthropod canopy fogging or sweep samples, and hypogean species, those living below the forest floor, could be sampled from the soil by Burlese or Winkler traps (Erwin 1996, Longino et al. 2002). Another advantage of such methods is the potential for enhanced statistical replication. For both canopy and soil collection methods samples could be taken from subplots within an altitudinal zone. For the present research, replications for hand collections were by sample date, and effort was not always even among samples. Experimental replication can also be improved by employing more than one altitudinal gradient. Although I employed two gradients for comparison of anthropogenic disturbance and old growth forests, a minimum of three gradients per treatment would be required for adequate statistical analysis. Given the limited altitudinal range sampled, which focused on carabid beetles of the cloud forest ecosystem (approximately 1400 m to 3450 m), we cannot predict the pattern of diversity if sampling was extended to the lowland forests of the Amazon basin 207 (approximately 300 m elevation). Extending collections at 500 m intervals along the length of the entire altitudinal gradient, including the lowest elevations, would obtain a more complete picture of how species richness varies with altitude (Rahbek 1995). Furthermore, a meta-analysis may be the next step in elucidating patterns of richness along an altitudinal gradient; McCain has presented altitudinal meta-analyses on bats (2007) and reptiles (2010). Although limited in scope, the comparison of carabid beetle assemblages between the Appalachian and Andes Mountains in Chapter VI was the first attempt at a regional scale analysis. Although there are limited altitudinal studies on carabid beetles, it would be useful to know how beetle assemblages respond to altitude in different geographic regions. In order to compare the carabid beetle assemblages over a long term census interval, I also suggest that this study be repeated in five to ten years. With the accelerated pace of climate warming and predicted decrease in global biodiversity (Coddington et al. 1999), it will be useful to examine how carabid beetles assemblages may be responding (e.g., upslope migration). Because changes in carabid beetle communities along an altitudinal gradient may reflect changes in other taxa, e.g., predators or prey, collaborative studies could also be conducted. Potential comparable taxa that have been documented along the same altitudinal gradient are dung beetles (Larsen 2012), termites (Palin et al. 2011), microbial community (Fierer et al. 2011) trees and birds (Jankowski et al. 2013), to name a few. Because I suggested that energetic constraints of the increasingly harsh abiotic environment play a role in changes in body length and dispersal ability of carabid beetles along an altitudinal gradient, physiological experiments in situ would be useful. 208 Comparing the respiration between high and low altitude species may help reveal if the physical environment is limiting flight capability or body size and if so, how. Furthermore, testing thermal tolerance would help determine potential ranges of species and understand how they might respond to climate change. Finally, with approximately 150 undescribed morphospecies, there are many potential classification and phylogenetic projects, which would provide detail to the diversity trends observed in this study. A better understanding of the phylogenetic relationships among the carabid beetles collected might also help reveal the biogeographic relationship of the Andean community to neighboring Amazonian taxa. 209 Literature Cited Brehm, G., D. Süssenbach, and K. Fiedler. 2003. Unique elevational diversity patterns of geometrid moths in an Andean montane rainforest. Ecography 26: 456-466. Coddington, J.A., C.E. Griswold, D. Silva Dávila, E. Peñaranda, and D.F. Larcher. 1991. Designing and testing sampling protocols to estimate biodiversity in tropical ecosystems. In The unity of evolutionary biology: Proceedings of the Fourth International Congress of Systematic and Evolutionary Biology. E.C. Dudley, Ed. Dioscorides Press, Portland: 44- 60. Erwin, T.L. 1996. Biodiversity at its utmost: tropical forest beetles. In Biodiversity II: understanding and protecting our biological resources. M.L. Reaka-Kudla, D.E. Wilson, and E.O. Wilson, Eds. Joseph Henry Press, Washington, D.C.: 27-40. Fierer. N., C.M. McCain, P. Meir, M. Zimmermann, J.M. Rapp, M.R. Silman, and R. Knight. 2011. Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92: 797-804. Jankowski, J.E., C.L. Merkord, W. Farfan Rios, K. Garcia Caberera, N. Salinas Revilla, and M.R. Silman. 2013. The relationship of tropical bird communities to tree species composition and vegetation structure along an Andean elevational gradient. Journal of Biogeography 40: 950-962. 210 Larsen, T.H. 2012. Upslope range shifts of Andean dung beetles in response to deforestation: compounding and confounding effects of microclimatic change. Biotropica 44: 82-89. Longino, J.T., J. Coddington, R.K. Colwell. 2002. The ant fauna of a tropical rain forest: estimating species richness three different ways. Ecology 83: 689-702 McCain, C.M. 2007. Could temperature and water availability drive elevational species richness patterns? A global case study for bats. Global Ecology and Biogeography 16: 1- 13. McCain, C.M. 2010. Global analysis of reptile elevational diversity. Global Ecology and Biogeography 19: 541-553. Palin, O.F., P. Eggleton, Y. Malhi, C.A.J. Girardin, A. Rozas-Dávila, and C.L. Parr. 2011. Termite diversity along an Amazon-Andes elevation gradient, Peru. Biotropica 43: 100- 107. Rahbek, C. 1995. The elevation gradient of species richness: A uniform pattern? Ecography 18: 200-205. Rahbek, C. 1997. The relationship among area, elevation, and regional species richness in Neotropical birds. American Naturalist 149: 875-902. 211 APPENDIX 212 Table A2. Summary of collection sites for Appalachian data set with corresponding altitude, latitude and longitude, forest type (HW: hardwood, SF: spruce-fir), and number of individuals (n) and species collected (S). Forest Altitude Altitude Latitude Longitude Locality Type (m) Band (m) (S) (W) n S Bradley Fork HW 675 600 35°33.182 083°18.702 323 17 Kephart HW 886 800 35°35.327 083°21.900 228 17 Quiet Walkway HW 1322 1400 35°35.962 083°24.847 251 18 Newfound Gap SF 1554 1600 35°36.617 083°25.823 777 23 Indian Gap SF 1722 1800 35°35.707 083°27.633 918 18 Clingman's Dome SF 1975 2000 35°33.473 083°29.690 1064 16 213 Table A3. Sampling effort for hand collections, based on person hours of collecting time, by altitudinal zone and collection year. See Table A1 for description of localities. 2007-08 Total Locality Altitude (m) 2010 2011 person Rainy Dry hours Pantiacolla 500 7.5 8 Tono 800 3 3 San Pedro 1400 4 10.5 9 3 27 Mirador 1750 4 5 9 Plot #8 1850 3.67 10.5 14 Plot #7 2000 4 3 7 Rocotal 2000 3 14 4 4.5 26 Plot #6 2250 3.33 7.5 11 Plot #5 2500 6 2 8 Pillahuata 2500 4 3.5 3 3 14 Plot #4 2750 7 8 15 Plot #3 3000 2 6 8 Wayqecha 3000 10 19.5 4.5 4.5 39 Plot #2 3250 5 6 11 Plot #1 3400 7 3.5 11 P.V. Acjanaco 3450 3 2 3 3.75 12 Tres Cruces 3650 8 3 11 214 215 216 217 218 219 220 221 222 223 224 Plate A1. Macropterous wing condition (wing state A: fully winged). Morphospecies Notiobia E (Tribe: Harpalini), 10 mm. Photo by K. N. Riley. 225 Plate A2. Brachypterous wing condition (wing state E: wing length ½ of elytron). Morphospecies Galerita A (Tribe: Galeritini), 19 mm. Inset: zoomed hind wing. Photo by S. A. Maveety. 226 Plate A3. Brachypterous wing condition (wing state G: wing stump). Morphospecies Dercylus A (Tribe: Oodini), A.B.L. 15.42 mm. Inset: zoomed hind wing stump. Photo by S. A. Maveety. 227 Plate A4. Micropterous wing condition (wing state H). Morphospecies Dyscolus A (Tribe: Platynini), 8 mm. Inset: zoomed hind wing nubbin. Photo by S. A. Maveety 228 Appendix A6: Diagnosis of Morphospecies. Organized alphabetically by Tribe, diagnoses includes morphospecies designation by genus, followed by average body length (ABL) across all localities (mm), altitudinal range (m), transect (D.: disturbed, O.G.: old growth, and P.: Pantiacolla), wing condition in italics (see Table V-1 for description), and description. ABL is the length from the extreme anterior part of the mandible to the extreme posterior part of the abdominal terga or elytra Wing states are given for di-/poly-morphic morphospecies and are as follows: A) full length folded wing; D) brachypterous wing length of the elytron; E) brachypterous wing ½ length of the elytron; F) brachypterous wing ¼ length of elytron; G) brachypterous wing stump; and H) micropterous wing pad. I. Bembidiini 1. Bembidion (Ecuadion) A. (3.55 mm, 500 m, P., Polymorphic-ADH. Similar to Bembidion A, but elytral punctures are deep and isolated in rows, otherwise glaborous dorsally. Legs rufotestaceous, head appendages flavous but darken apically. 2. Bembidion A. (3.87 mm, 2000 m ‒ 3000 m, D., O.G., Dimorphic-AH. Body infuscate. Palpomeres 3 and 4 infuscate. Frontal grooves slightly furrowed. Pronotum with lateral margin sinuate basally, hind angle acute, basal impression linear and deep. Elytral interneurs striatiopunctate basally, effaced apically. Appendages rufotestaceous, infuscate apically. 3. Bembidion D. 3.80 mm, 2250 m ‒ 3450 m, D., O.G., Micropterous. 229 Pronotum with lateral margin sinuate, hind angle obtuse. Elytra rotund, interneurs effaced through entire length, except for the regular setae on interneur 3. Appendages bicolored. 4. Bembidion E. 4.39 mm, 2500 m ‒ 3450 m, D., Polymorphic-AGH. Body black with varying iridescence. Head appendages testaceous [scape rufotestaceous, flagellum rufoinfuscate]. Pronotum cordate, hind angle square; basal impression extended laterally across the base (not elevated by suture at middle). Elytron glossy. Legs bicolored [tarsus basally testaceous, tibia light rufotestaceous, base of femur and trochanter testaceous]. 5. Bembidion F. 5.20 mm, 2000 m – 3000 m, D., Polymorphic-AGH. Palp darkly infuscate. Pronotum with lateral margin sinuate, hind angle slightly acute. Elytron slightly glittery green iridescent but matte; interneurs striatiopunctate. Legs brown- flavous (infuscate apically). 6. Bembidion G. 3.48 mm, 1750 m ‒ 3000 m, D., Micropterous. Pronotum with lateral margin sinuate, hind angle obtuse. Elytron slightly iridescent purple; interneurs effaced except for recurrent groove. All appendages testaceous (except coxa infuscate). 7. Bembidion H. 6.04 mm, 2000 m ‒ 2500 m, D., Dimorphic-AH. Antennae infuscate. Pronotum with lateral margin sinuate, hind angle rectangular; basal impression somewhat foveate. Elytron green; interneurs slightly striatiopunctate. Legs bicolored. 8. Bembidion I. 4.16 mm, 2500 m, D., Dimorphic-GH. 230 Frontal furrows markedly impressed, extended to basal 1/3 of eye. Antenna infuscate apically. Pronotum rounded, lateral margin sinuate, hind angle acute. Elytral interneurs striatiopunctate, scutellum rounded. Appendages pale yellow. 9. Bembidion K. 5.16 mm, 2000 m, D., Dimorphic-AH. Body infuscate, short and ovoid. Mouth parts darker than legs. Pronotum with hind angle slightly acute; basal impression deep. Elytral margins parallel, interneurs shallow, recurrent groove striatiopunctate. Legs rufotestaceous. 10. Bembidion L. 4.23 mm, 3000 m ‒ 3450 m, D., Dimorphic-GH. Body black. Pronotum with lateral margin sinuate; hind angle acute, almost toothed. Elytral interneurs shallow, scutellar interneurs striatiopunctate. Legs infuscate, slightly rufous at all joints. 11. Bembidion M. (4.88 mm, 3000 m, D., Micropterous). Body black-brown, margin slightly testaceous (if not lighter). Pronotum with lateral margin sinuate, hind angle obtuse; basal impression deep. Elytral interneurs completely striatiopunctate. Legs brown- flavous. 12. Bembidion N. 4.29mm, 3450 m ‒ 3650 m, D., O.G., Dimorphic-AH. Hind angle rectangular, basal impressions deeply ovate. Elytral process similar to Bembidion L. Legs dark but lighter apically, with trochanters flavous. 13. Bembidion O. 4.15mm, 3650 m, O.G., Micropterous. Scape lighter ventrally only. Pronotum sinuate, basal impressions deep and reach lateral margin with slight carina between impression and margin. Legs dark, trochanter and tibia-tarsus almost flavous, coxae lighter. 14. Bembidion P. 3.00 mm, 3400 m, O.G., Micropterous. 231 Antennomeres brown, except flavous basally (more flavous towards base of antenna and more brown towards apex). Palps flavous except maxillary palpomere 3 darker. Mandibles bicolored, lighter apically. Hind angle obtuse. Elytra completed effaced except for usual 3 setae. Tibia and trochanter flavous, otherwise legs brown. 15. Bembidion Q. 4.88 mm, 3000m – 3400 m, O.G., Micropterous. Body black. Antennae rufotestaceous; maxillary palps same color (slightly darker apically) and labial palps darker. Pronotum cordate with deep short linear basal impressions, hind angle acute. Elytral pattern with white markings (See Figure A1-A), interneurs punctate throughout. Legs same color as body basally but become lighter apically until tarsi almost flavous. 16. Bembidion R. 5.36 mm, 2750 m ‒ 3400m, O.G., Micropterous. Body black-brown. Antennae flavous, mandibles light, and palps flavous but dark brown apically. Cordate pronotum, widest at apical 1/3; hind angle obtuse with flattened margin; basal impressions linear. Pronounced humeral margin, close to being dentate. Elytral pattern with white markings (See Figure A1-B) that vary by individual; interneurs moderately deep and punctate. Legs flavous but darker basally, and coxae same color as body. 17. Bembidion U. 3.79 mm, 2000 m, D., Macropterous. Very similar to Bembidion A, but striatiopunctate to middle of elytron. Flavous appendages are all darker basally. Species more bulky than B. A. 18. Bembidion V. 4.69mm, 2000 m, D., Micropterous. 232 Very similar to Bembidion K, but elongate. Antennomeres brown, except flavous basally (more flavous towards base of antenna and more brown towards apex). Pronotum with hind angle rectangular Slight green iridescence. Legs pale yellow. 19. Meotachys A. 1.94 mm, 500 m, P., Macropterous. Body brown-flavous. Antennae flavous except antennomeres 2-6, darker. Pronotum with hind angle obtuse. Elytra with slight rainbow iridescence, and darker along outer margins and medial suture. Legs flavous. 20. Paratachys A. 3.05 mm, 1750 m, D., Macropterous. Body brown. Appendages lighter to flavous; terminal palpomeres almost translucent. Eyes large. Pronotum with hind angle reflexed and obtuse. Elytral interneurs effaced. 21. Paratachys B. 2.69 mm, 1750 m, D., Macropterous. Body flavous-brown. Similar to Paratachys A in shape, but color different. II. Cicindelinae 22. Pseudoxycheila lateguttata peruviana Cassola 1997. 17.15 mm, 2000 m, D., Macropterous. Erwin, T.L. & Pearson, D.L. 2008. A Treatise on the Western Hemisphere Caraboidea (Coleoptera): Their classification, distributions, and ways of life Volume II (Carabidae – NEBRIIFORMES PART 2). 400 pp. 33 plates. Pensoft, Sofia-Moscow. III. Clivinini 23. Ardistomus A. 6.32 mm, 1400 m, D., Macropterous. Body dark black. Mouthparts rufotestaceous, legs testaceous. 24. Aspidoglassa A. 4.97mm, 500 m, P., Macropterous. 233 Body brown. Pronotum circular. Elytra striatiopunctate from base to middle. 25. Clivina A. 8.13 mm, 800 m, D., Macropterous. Body red, except pronotum and head darker black. Pronotal anterior angle somewhat pointed. Elytral interneurs completely punctate. 26. Clivina B. 16.20 mm, 800 m, D., Macropterous. Head with large punctures and sulcus. Basal and lateral margins of elytra densely punctate. 27. Clivina C. 7.14 mm, 500 m, P., Macropterous. Body brown. Pronotum square, at least twice as large as head. Elytra punctate basally (to middle), margin pale. 28. Clivina D. 12.92 mm, 500 m, P., Macropterous. Body completely black, except antennae flavous. Almost like a small version of Clivina B, but mandibles different. 29. Nyctosyles A. 10.20 mm, 500 m, P., Macropterous. Body completely black, except head appendages somewhat red. Mandibles small. Pronotum proportionately large and flat, hind angle obsolete. Elytral interneurs punctate. *new species. IV. Galeritini 30. Galerita A. 19.06 mm, 1750 m ‒ 2000 m, D., O.G., Brachypterous-EF. Body uniformly infuscate. Head, pronotum with long sparse setae. Antenna, tarsus apically rufotestaceous (from antennomere 5 and tarsomere 5). Pronotum with hind angle acute, slightly elevated. Elytral interneurs with reduced carinae and short setae. See Appendix Plate 1 for wing state. 234 31. Galerita B. 18.31 mm, 1400 m – 1850 m, D., O.G., Brachypterous-EF. Body dark, entirely setose dorsally. Antenna bicolored [1-4: rufous, remaining flagellum testaceous, except apical third of antennomere 5-8 infuscated]. Pronotum sinuate, hind angle acute. Elytral pattern almost the same as Galerita A with interneurs more shallow. Front tarsomeres articulated obliquely in males. 32. Galerita C. 19.82 mm, 2000 m, D., Brachypterous-E. Body uniformly brown, dull matte. Antennal flagellum and venter of tarsomeres paler. Head, pronotum punctuate, not densely setose. Leg with testaceous setae. Elytron with interneurs carinate, interneurs normal, shallow; elytral setae sparse, regular. 33. Galerita D. (17.00 mm, 2000 m, D., Brachypterous-E. Similar to Galerita C, with pronotum glabrous, elytral disc (close to suture) glabrous. 34. Galerita E. 19.55 mm, 500 m, P., Brachypterous-G. Body black with ventral flavous setae. Antennomeres 1-4 black, 5-11 lighter. Head and pronotum punctate. Pronotum sinuate, widest at apical 1/3 and hind angle elevated laterally and quadrate. Elytra costate with slight turquoise shimmer when dry. 35. Galerita F. 19.41 mm, 1850 m, O.G., Brachypterous-E. Broad forebody and head. Pronotum with hind angle quadrate, barely sinuate (otherwise similar to Galerita A). Abdomen more pubescent. 36. Galerita G. 19.09 mm, 1750 m ‒ 1850 m, D., O.G., Brachypterous-E. Pronotum sinuate, hind angle seems reflexed outward and down into acute angle. 235 37. Galerita H. 17.81 mm, 500 m, P., Dimorphic-AG. Body black with ventral golden setae that give abdomen a distinct look, dorsal surface with only short pubesence. Antennal process similar to Galerita E. Pronotum sinuate, and hind angle smoothly acute. V. Harpalini 38. Athrostictus A. 11.81 mm, 800 m, D., Macropterous. Black and completely setose dorsally (head with only patchy setae); ventrally – rugous. Mouthparts light. Pronotum with hind angle rounded. Legs black, tarsi lighter, almost reddish. 39. Athrostictus B. 9.56 mm, 500 m, P., Macropterous. Black with slight rainbow iridescence, completely setose. Dorsal setae flavous. Labrum extends almost to tip of mandibles. Pronotum slightly sinuate basally, with hind angle rounded quadrate, lateral margin translucent. Appendages all flavous, except coxae and hind trochanter brown. 40. Goniocellus A. 3.75 mm, 2500 m, D., Macropterous. Body black. Antenna testaceous. Pronotum with lateral bead complete, hind angle rectangular with rufous translucence. Elytral intervals flat, deeply striatiopunctate. Appendages pale yellow. 41. Notiobia A. 8.93 mm, 1400 m, D., Macropterous. Elytron slightly purple, pronotum slightly green. Eyes large, round. Mouthparts testaceous. Pronotum with lateral margin dark flavous, slightly raised. Legs infuscate. 42. Notiobia B. 9.03 mm, 1400 m, D., Macropterous. 236 Head smaller, eyes large. Pronotum with marked basal impressions linear, lateral margin slightly translucent that widens basally. Elytron with distinct interneurs, deeply striatiopunctate. Appendages pale yellow. 43. Notiobia C. 7.24 mm, 1400 m ‒ 1750 m, D., Macropterous. Pronotum with lateral margin slightly sinuate, hind angle acute (this is the difference between morphospecies B and C). Elytron similar to Notiobia B. All appendages the same as Notiobia B also. 44. Notiobia D. 8.92 mm; 1400 m, D., Macropterous. Pronotum with lateral margin sinuate, uniformly wide and translucent, hind angle rectangular-acute. Elytron with golden luster. Appendages testaceous, legs paler. 45. Notiobia E. 10.10 mm, 1400 m ‒ 2000 m, D., O.G., Macropterous. Pronotum with lateral margin slightly elevated, wide at base, translucent; basal impression shallow; hind angle acute-rectangular. Elytron slightly green, matte; intervals flat. Appendages testaceous. 46. Notiobia F. 11.22 mm, 1400 m ‒ 2000 m, D., Macropterous. Antennomeres darker basally in 1-3, antennomeres from 4 on have a dark dorso- lateral streak. Palpi testaceous. Bead of pronotum complete, lateral margin sinuate and rufous, hind angle rounded; basal impression shallow. Elytra iridescent green- purple; intervals flat, barely striatiopunctate. Legs infuscate, except coxae and trochanters flavous apically. Sexually dimorphic (female with dull matte). Color varies between individuals because it appears to take a long time to fully become pigmented after adult eclosure. 47. Notiobia H. 9.81 mm, 1400 m, D., Macropterous. 237 Body rufous ventrally, black dorsally. Antenna rufous apically; palp testaceous. Pronotum with lateral margin sinuate, hind angle rectangular; basal impression linear, deep. Elytron with deep interneurs. Legs black, rufous apically. 48. Notiobia I. 10.35 mm, 1400 m ‒ 2000 m, D., Macropterous. Pronotum with lateral margin sinuate, hind angle acute-rectangular, margin slightly translucent. Elytral interneurs shallow, dull matte. All appendages uniform rufotestaceous. 49. Notiobia J. 11.05 mm, 1400 m, D., Macropterous. A slender species (as compared to the normal wide Harpaline look). Body rufous ventrally. Palp testaceous. Pronotum with lateral margin sinuate, rufous translucence, hind angle rectangular; basal impression punctuate. Elytron with interneurs deep, slightly striatiopunctate. Appendages rufous. 50. Notiobia K. 13.81 mm, 2000 m, D., Macropterous. Body all black. Antenna black basally, palp bicolored. Pronotum with lateral margin slightly elevated, hind angle obtuse; basal impression shallow. Elytral interneurs shallow. Legs black, tarsus rufous. 51. Notiobia M. 11.57 mm, 900 m, P., Macropterous. Dorsal surface completely metallic brassy. Pronotum sinuate, hind angle obtuse, lateral bead complete to hind angle. Appendages brown, trochanters, tarsi lighter. 52. Notiobia N. 8.82 mm, 500 m, P., Macropterous. Pronotum widest at apical 1/3, lateral margin translucent, hind angle obtuse, base of pronotum seems lightly punctate. Elytra with rainbow and green iridescence, 238 appears quadrate, interneurs completely punctate. Appendages completely flavous, except joints on legs darker. 53. Notiobia O. 13.34 mm, 500 m, P., Macropterous. Body black, and shape similar to Notibia M. Pronotum sinuate and hind angle acute, lateral margin widened (flat). Intervals on elytra elevated. All appendages dark, except ultimate palpomeres and terminal tarsomeres. 54. Pelmatellus A. 5.07 mm, 2000 m, D., Macropterous. Body infuscate. Antenna, mouthparts testaceous. Pronotum with medial setae on lateral margin, hind angle obtuse. Elytron with interneurs glabrous, shallow. Legs pale yellow. 55. Pelmatellus C. 6.39 mm, 2000 m ‒ 3000 m, D., Polymorphic-AGH. Body black-brown. Antennae light, especially testaceous basally. Pronotum with hind angle obtuse, rounded, almost obsolete; lateral bead complete, margin slightly rufous, basal impressions shallow. Elytron with interneurs shallow; base of elytra wider than base of pronotum. Appendages completely testaceous, legs infuscate basally, lighter at joints. 56. Pelmatellus D. 6.04 mm, 2500 m ‒ 3000 m, D., Micropterous. Body black. Mouthparts testaceous. Pronotum with hind angle completely rounded, lateral margin widens basally. Elytron slightly iridescent; interneurs shallow, intervals elevated, slightly striatiopunctate. Legs pale yellow, infuscate basally. 57. Pelmatellus E. 5.26 mm, 2500 m ‒ 3250 m, D., O.G., Micropterous. 239 Pronotum with hind angle rounded, lateral margin translucent. Elytron with rainbow iridescence; interneurs striatiopunctate, intervals flat. Appendages testaceous. 58. Pelmatellus F. 5.42 mm, 1400 m, D., Macropterous. Body brown. Pronotum with hind angle rectangular, translucent; lateral bead ends anterior to hind angle. Elytral interneurs almost invisible, striatiopunctate. Appendages testaceous, except for the coxa. 59. Pelmatellus G. 7.21 mm, 1400 m, D., Macropterous. Body dark brown. Mandibles testaceous. Pronotum with lateral margin testaceous, hind angle acute-rectangular. Elytron with rainbow iridescence; interneurs shallow, slightly striatiopunctate, deeper apically. Appendages testaceous. 60. Pelmatellus H. 6.59 mm, 2500 m ‒ 3000 m, D., Macropterous. Similar in shape to Pelmatellus C. Head appendages rufous. Pronotum with hind angle acute-rectangular, lateral margin flat; basal impression shallow. Legs almost completely black, rufous setae. 61. Pelmatellus I. 9.67 mm, 1400 m, D., Macropterous. Also similar to Pelmatellus C except larger in size and found at lower elevation. Pronotum with hind angle obtuse, slightly toothed; basal impression linear, slightly punctate at the hind angle. Legs rufous anterior to femora. TRAP ONLY. 62. Pelmatellus J. 6.67 mm, 2500 m ‒ 3650 m, D., O.G., Macropterous. Body entirely black. Palp brown-testaceous. Pronotum with hind angle acute. Elytra wider than pronotum; interneurs shallow, slightly striatiopunctate. Legs with rufous setae, trochanter rufous. 240 63. Pelmatellus K. 5.22 mm, 2000 m, D., Macropterous. Antenna brown. Pronotum with hind angle obtuse, rounded, lateral bead complete. Elytron with intervals flat, interneurs shallow. Appendages pale yellow, except coxae darker than the rest of the legs. 64. Pelmatellus L. 11.56 mm, 2500 m ‒ 3000 m, D., Macropterous. Body markedly black. Palpomere, antennomere apically rufous. Pronotum with wide lateral bead, hind angle obtuse, rounded. Elytron metallic purple-blue. Tarsus rufous. 65. Pelmatellus M. 6.31 mm, 3250 m ‒ 3650 m, O.G., Micropterous. Body black. Pronotum widens apically with hind angle obtuse, rounded, almost obsolete; lateral bead complete, margins (including basal) slightly translucent. Elytron with interneurs shallow; base of elytra wider than base of pronotum. Appendages completely testaceous, except coxae. 66. Pelmatellus N. 6.26 mm, 1400, D., Macropterous. Head and pronotum rufous. Pronotum sinuate and hind angle rectangular. Elytra black with shallow interneurs. Appendages flavous, ventral surface very red. 67. Selenophorus A. 10.08 mm, 500 ‒ 1750 m, D., P., Macropterous. Small mandibles, not much longer than labrum. Appendages testaceous. Pronotum basally punctuate, hind angle obtuse, rounded, and lateral margins slightly translucent. Ventral sternites setose. Elytra with rainbow iridescence, interneurs well defined. Legs pale yellow (longitudinally proximally infuscate). 68. Selenophorus B. 10.28 mm, 500 m ‒ 1400 m, D., P., Macropterous. 241 Same as Selenophorus A but femora NOT proximally infuscate and femora dilated. 69. Selenophorus C. 7.25 mm, 500 – 1400m, D., P., Macropterous. Colors, appearance, similar to Selanophorous A., except legs entirely flavous and pronotal angle rectangular-acute, margins very translucent and then widens towards hind angle. Interneurs slightly punctate. 70. Selenophorus D. 7.53 mm, 500m –1750 m, D., P., Micropterous. Overall brown-red. Appendages dark flavous. Pronotum widest at apical 1/3, but quadrate, hind angle rounded/obtuse, no basal impressions. Elytra with interneurs almost obsolete, and rainbow iridescence. 71. Selenophorus E. 5.12 mm, 1400 m, D., Macropterous. Abdomen and elytra very dark brown. Head, pronotum, legs (except coxae) uniform orange flavous. Antennomeres 1-3 flavous, (3 darkens apically), 4-11 dark. Hind angle obtuse, lateral margin flattened. Very distinct. 72. Selenophorus F. 9.00 mm, 500m, P., Macropterous. Body completely black, broad. Head appendages and tarsi lighter orange. Pronotum twice as wide as long and proportionately large. Elytral interneurs deep and punctate. Robust like an Oodini. 73. Trichopselaphus A. 9.99 mm, 1400 m, D., Macropterous. Left mandible larger in size than the right. Pronotum with lateral margin elevated, slightly translucent. Elytron with rainbow iridescence; interneurs shallowly striatiopunctate. Legs pale yellow. TRAP ONLY. 74. Trichopselaphus B. 10.52 mm, 1400 m, D., Macropterous. 242 Similar to Trichopselaphus A, except pronotum with lateral bead rufous (similar to appendages). Head apically, pronotum basally punctate. TRAP ONLY. VI. Hilitini 75. Eucamaragnathus batesii (Chaudoir, 1861). 9.56 mm, 500 m, P., Brachypterous- G. Erwin, T.L., Stork, N. 1985. The Hiletini, an ancient and enigmatic tribe of Carabidae with a pantropical distribution (Coleoptera). Systematic Entomology 10(4):405-451. VII. Insertae sedis 76.Andinodontis maveetyae (Erwin and Maddison, 2010). 2.21 mm, 1750 m ‒ 2000m, D., O.G., Dimorphic-AG. Erwin, T.L., Toledano, L., Maddison, D.R. 2010. New enigmatic species of ground beetles from stream margins and scree in the Andes of South America (Carabidae, Trechitae, Andinodontis n. gen.). Entomologische Blätter 106:73:88. VIII. Lachnophorini 77. Anchonoderus A. 6.68 mm, 1750 m ‒ 2000 m, D., Macropterous. Body dark brown. Completely setose ventrally, all appendages pale yellow. 78. Anchonoderus B. 5.99 mm, 1400 m ‒ 2000 m, D., Macropterous. Body metallic blue. Pronotum with hind angle rectangular. Head appendages testaceous, legs apically lighter. Elytron striatiopunctate. Otherwise markedly similar to Pseudophorticus A. 79. Eucaerus A. 5.84 mm, 500 m, P., Brachypterous-E. 243 Body black. Antennomeres 1-2 rufous, 3-4 black, 5-11 white (11 slightly darker). Head and pronotum with coarse microsculpture (large pores). Pronotum cordate, hind angle obsolete except for slight articulation at hind angle. Elytra with rainbow iridescence and deep interneurs. Legs flavous. 80. Pseudophorticus A. 5.47 mm, 1400 m ‒ 2000 m, D., Macropterous. Body black, dorsally punctate. Head appendages light rufous. Pronotum broad with sharp hind angle acute. Elytra and pronotum rugose. 81. Pseudophorticus C. 5.33 mm, 1400 m, D., Macropterous. Body rugose. Pronotum cordate, hind angle rectangular-obtuse. Elytra randomly pictured (may be represented by teneral specimen). Legs pale yellow. 82. Pseudophorticus D. 5.64 mm, 1400 m, D., Macropterous. Forebody with slight green/blue iridescence. Appendages orange. Mandibles long. Pronotum circular except for rectangular hind angle. Elytra black. Hind trochanters dark. 83. Pseudophorticus E. 6.71 mm, 500 m, P., Macropterous. Body black. Head appendages orange-flavous. Head punctate basally. Pronotum cordate, base about ½ the width of apical 1/3, hind angle quadrate-obtuse. Pronotum and elytra densely punctate. Elytra white marks as Figure A1-C. Legs pale yellow (joints darker). 84. Pseudophorticus F. 7.36 mm, 500 m, P., Macropterous. Body black. Antennomeres 1-4 flavous, 5-11 infuscate. Pronotum less wide than elytra, sinuate and hind angle rectangular/obtuse, pronotal setae long. Elytron 244 with white spot in apical third (lateral middle), size varies by individual. Legs pale yellow. 85. Pseudophorticus G. 5.23 mm, 500 m, P., Macropterous. Body black with gold/metallic luster. Appendages rufo-testaceous basally, darker apically. Head setose. Pronotum with basal margin literally obsolete. Elytral spots similar to Pseudophorticus E. IX. Lebiini 86. Apenes A. 7.58 mm, 1850 m, O.G., Macropterous. Appendages flavous. Pronotum cordate, margins translucent, hind angle obtuse with slight bump at setae. Elytra dark with one basal and one apical spot (see Figure A1-D). Legs pale yellow. 87. Apenes B. 4.85 mm, 1400 m – 1850 m, D., OG , Macropterous. Body completely rufo-testaceous except for elytra, which is completely dark brown with margins flavous. Labrum appears Scaraboid, larger (~2x) than clypeus. Eyes small, flat. Pronotum approx. twice wider than long, hind angle obsolete (broad anteriorly, markedly narrowed to base), margin angulate at apical 1/3, straight posteriorly. Elytral margins parallel. 88. Apenes C. 6.42 mm, 500 m, P., Macropterous. Head appendages rufo-testaceous. Mandibles long. Pronotum cordate with lateral and basal margins somewhat flattened and punctate, wrinkled; hind angle acute with tiny tooth. Elytra with gold luster and spots like Figure A1-E, interneurs deep. Legs pale yellow. 89. Apenes D. 8.12 mm, 900 m, P., Macropterous. 245 Similar to Apenes C, but forebody also metallic and not wrinkled. Larger and broader body. Appendages dark flavous (almost orange). Ultimate labial palpomeres triangulate. Mandibles short. Elytron with apical spot at lateral middle (spans 2 interneurs) and interneurs punctate. 90. Calleida A. 12.06 mm, 1750 m ‒ 2000 m, D., Macropterous. Body infuscate, glabrous; dorsally green-pink metallic. Antennomere 1-2 testaceous, antennomere 4 basally testaceous, otherwise antenna infuscate. Femur same color as elytron; tibia and tarsus testaceous, tarsomere 3-5 infuscate. Palp infuscate. Pronotum with lateral margin sinuate, hind angle rectangular, punctate basally. Elytron metallic green; interneurs shallowly striatiopunctate. ARBOREAL. 91. Calleida B. 11.47 mm, 1400 m, D., Macropterous. Body completely testaceous. Pronotum with lateral margin sinuate, completely elevated, translucent; hind angle rectangular-obtuse. Elytron metallic green-pink; interneurs shallow, striatiopunctate. Intervals 6&7 with elevated carinae in basal third. 92. Lebia A. 6.98 mm, 3000 m, D., Macropterous. Body brown. Antenomere 3 and 4 basally infuscate, palp testaceous. Pronotum with hind angle obtuse, elevated. Elytron at apical third at least twice the width of the head; interneurs normal. Legs testaceous-brown. 93. Lebia B. 5.04 mm, 1400 m, D., Macropterous. Body testaceous; elytra with two broad brown bands. Appendages testaceous. Pronotum with hind angle square, elevated – margin fully translucent (pale 246 yellow). Elytron at apical third slightly wider than head across eyes; intervals moderately convex. 94. Lebia C. 6.23 mm, 3250 m, O.G., Macropterous. Body completely brown. Frons before clypeus has an upward “V” which separates dark brown head from flavous (inside V and) clypeus. Appendages testaceous, legs slightly darker basally. Pronotum with hind angle square, but rounded and elevated (rest of margin elevated but slightly less). Abdomen pubescent. Elytra translucent flavous with symmetrical black spots (interneurs shallow). See Fig A1-F. 95. Lebia D. 6.39 mm, 1850 m ‒ 3250 m, O.G., Macropterous. Similar to Lebia C, but with extra spot in the base of the elytra, and apical spot is extended to edges. Pronotum margin more elevated. See Fig A1-G. 96. Lebia E. 6.00 mm, 1750 m, D., Macropterous. Body and appendages flavous. Pronotum with margin wide and completely flattened (translucent); hind angle rounded but rectangular. Elytra black except apical margin testaceous, with white spot in apical 1/3 (lateral center, spans 5 interneurs). X. Megacephalini 97. Tetracha spixi (Brullé, 1837). 17.47 mm, 800 m, D., Macropterous. Erwin, T.L. Pearson, D.L. 2008. A Treatise on the Western Hemisphere Caraboidea (Coleoptera): Their classification, distributions, and ways of life Volume II (Carabidae – NEBRIIFORMES PART 2). Pensoft, Sofia-Moscow. 400 pp. 33 plates. 247 XI. Odacanthini 98. Colliuris A. 9.36 mm, 1750 m, D., Macropterous. Body black. Antennae flavous, mouthparts black. Pronotum with lateral ridges through extent of pronotum, greenish metallic luster. Symmetric white spots on elytra, one in basal third spans interneurs 3-6, one in apical third spans interneurs 4-7. Long setae interspersed across elytra. Legs flavous, except for apical half of hind femora dark.. 99. Colliuris B. 6.42 mm, 800 m, D., Macropterous. Body black. Scape brown, antennomeres 2-4 pale yellow, and 5-11 black. Head and pronotum with metallic green tint. Pronotum bulbous in basal third, narrowing again at base (fusiform). Lateral margins of elytra translucent, and elytral spots similar to Colliuris A, but fainter. Legs pale yellow except apical half of all femora black, then tibiae and tarsi more brown. XII. Oodini 100. Dercylus A. 15.06 mm, 500 m – 1400 m, P., D., Brachypterous-G. Body black. Head with deeply grooved frons, eyes large. Mandibles short with dorsal striations, left mandible with hook. Maxillary palp basally tapered. Pronotum with lateral bead complete, hind angle with seta; basal impression linear, deep. Elytron with interneurs markedly striatiopunctate. (For wing state, see Plate 2, Appendix) XIII. Ozaenini 101. Pachyteles A. 8.07 mm, 1400 m, D., Micropterous. 248 Body red-brown, ovate. Head wrinkled. Pronotum with hind angle rectangular. Elytral interneurs nearly effaced, striatiopunctate. Appendages rufotestaceous (except antenna). 102. Pachyteles B. 9.24 mm, 1400 m, D., Macropterous. Body dark brown dorsally, narrowly elongate. Head appendages rufous. Pronotum small with hind angle rectangular; lateral margin sinuate, elevated along entire length, “wavy” apically; pronotum with sharp apical angle. Elytron with interneurs effaced, hardly visible. Legs testaceous. Femoral spine less sharp than other P. spp. 103. Pachyteles C. 9.38 mm, 1400 m – 1750 m, D., Macropterous. Similar to Pachyteles B overall. Body less dark dorsally. Pronotum with lateral margin “wavy” over entire length, hind angle rectangular, number of setae along lateral margin = 7. Femoral spine sharp. XIV. Perigonini 104. Diploharpus A; (8.38 mm, 2000 m, D., Macropterous. Body brown. Mandibles long. Pronotum with lateral margin elevated, wider basally, hind angle obtuse with a smoothed tooth. Elytron with rainbow iridescence, interneurs nearly effaced. All appendages testaceous (almost “pumpkin” colored) except coxa infuscate. XV. Platynini 105. Dyscolus A. 7.64 mm, 2500 m ‒ 3450 m, D., O.G., Polymorphic-AEFH. Mouthparts testaceous, antennomeres testaceous from 3 to apex. Pronotum with hind angle rounded, basal impressions small circular and almost obsolete. Elytron 249 with interneurs effaced except for the normal setae (interval 3); humeral margin noticeable. Legs testaceous from tibia to tarsus. (For wing state, see Plate 3, Appendix). 106. Dyscolus B. 5.81 mm, 2500 m ‒ 3400 m, D., O.G., Micropterous. Palp lighter than other appendages. Pronotum elongate, oval, hind angle obtuse, slightly obsolete; lateral bead complete. Elytra ovate, base narrow, slightly pointed humeral angle. All appendages uniformly dark testaceous. 107. Dyscolus C. 8.82 mm, 3000 m – 3450 m, D., Micropterous. Pronotum with lateral margin sinuate, hind angle obtuse. Elytral interneurs slightly striatiopunctate. All appendages testaceous, legs testaceous from tibia to apex. Femora infuscate. 108. Dyscolus D. 6.22 mm, 2500 m ‒ 3450 m, D., Polymorphic-AEFH. Pronotum with a rounded quadrate shape, hind angle obtuse, basal impression linear. Elytron convex. Appendages testaceous, femur rufous. 109. Dyscolus E. 10.06 mm, 1750 m ‒ 3450 m, D., O.G., Micropterous. Mandibles long. Pronotum with hind angle almost square, lateral margin basally sinuate. Elytral interneurs shallowly striatiopunctate. Similar color scheme in appendages as in Dyscolus A and Dyscolus C. 110. Dyscolus F. 6.94 mm, 3450 m ‒ 3650 m, D., O.G., Polymorphic-AEF. All appendages bi-colored (femora dark, tibiae and tarsomeres flavous basally and darker apically, coxae lighter; antennomeres dark but small flavous band basally; palpomeres dark but flavous apically). Pronotum rounded, slight bump 250 on margin at basal puncture, basal impressions almost obsolete but linear and long, appears flattened to lateral margin. 111. Dyscolus G. 7.58 mm, 2000 m ‒ 3000 m, D., Macropterous. Head narrower across eyes than elytra. Forebody blue-greenish. Pronotum with lateral margin sinuate and reflexed; basal impression deep, wrinkled. Elytron iridescent purple, elytral humerus rounded. Legs infuscate like the rest of body, lighter apically. 112. Dyscolus H. 10.09 mm, 2500 m, D., Micropterous. Body uniformly red-brown. Mouthparts, antenna testaceous. Pronotum with lateral margin slightly sinuate towards the obtuse hind angle. Elytra broad (rotund), interneurs slightly striatiopunctate. Legs testaceous only at joints. [Singleton, could be a teneral individual as it does not seem fully scleritized]. 113. Dyscolus J. 14.02 mm, 1850 m, O.G., Macropterous. Mandibles long. Pronotum round (almost circular), lateral margin slightly sinuate before hind angle, elevated; basal impression deep. Elytron with blue-rainbow iridescence; interneurs deep, slightly striatiopunctate. Appendages apically rufotestaceous, all black otherwise. 114. Dyscolus L. 9.37 mm, 3450 m, D., Macropterous. Body black. Pronotum wide, lateral margin sinuate basally. Elytral interneurs hardly striatiopunctate. All appendages testaceous, except coxa darker. Rotund like a Harpaline. 115.Dyscolus M. 8.47 mm, 3000 m, D., Micropterous. 251 Head, pronotum narrow. Elytron with interneurs deeply striatiopunctate. Legs testaceous from tibia to apex, legs long; all other appendages testaceous. 116. Dyscolus O. 12.59 mm, 1400 m – 2000 m, D., Macropterous. Forebody red. Palps rufotestaceous, Antennomeres 1-3 glabrous, 4-11 setose (#4 glabrous in apical 1/3); antennomeres 1-4 brown but rufous at joints, 5-11 lighter (flavous). Pronotum with lateral margin flattened along entire length, sinuate, hind angle rectangular; basal impression deep and toward margin. Elytra with green luster. Legs dark, coxae and tibiae red, black spots on tarsomeres 3 and 4. 117. Dyscolus Q. 7.77 mm, 1400 m, D., Micropterous. Body brown. All appendages flavous (legs darker). Pronotum cordate and proportionally large; hind angle rectangular, widest at middle; basal impressions deep and lateral. Elytra round, with slight iridescence or dull matte (sexually dimorphic). 118. Dyscolus R. 7.74 mm, 500 m, P., Micropterous. Body brown. Appendages orange-flavous. Pronotum circular, somewhat sinuate, hind angle obtuse . 119. Glyptolenus A. 7.49 mm, 2000 m ‒ 3000m, D., O.G., Dimorphic-AC. Body completely black ventrally, metallic blue dorsally. Palpomere 4 testaceous in apical third. Pronotum with lateral margin elevated basally; basal impression deep. Elytron iridescent green-blue; interneurs thin, shallow, intervals flat. Appendages same color as body, apically becomes rufous-testaceous because of testaceous setae. 120. Glyptolenus B. 6.28 mm, 2500 m, O.G., Brachypterous-E. 252 Similar in shape and color to Lebiini. Head red and forebody shiny black. Mandibles long. Antennae very flavous, maxillary palps somewhat bicolored and labial palps darker. Pronotum rounded, margin flattened across length (but thin) hind angle rounded and slightly elevated at setae. Elytra with slight green metallic luster and glabrous except for normal setae (wider than pronotum), interneurs shallow and slightly punctate. Legs flavous except for basal 2/3 of femora and coxae. 121. Glyptolenus C. 6.54 mm, 1750 m ‒ 1850 m, D., O.G., Macropterous. Similar to Glyptolenus B but bicolored: head red and pronotum black. All appendages flavous. Hind angle obtuse, reflexed margins. 122. Glyptolenus D. 8.31 mm, 1400 m, D., Macropterous. Body brown. Antennae flavous, palps lighter. Clypeus deeply grooved. Pronotum distinct, completely wrinkled laterally, broad anteriorly, and sinuate to base; side angulate at middle. Hind angle rectangular. 123. Glyptolenus E. 7.34 mm, 1850 m, O.G., Micropterous. Body brown-flavous. Appendages flavous. Head almost red, deep frontal furrows. Pronotum large and circular, sinuate through base, hind angle rectangular. 124. Platynus A; 12.57 mm, 2000 m, D., Macropterous. Body black. Mandibles long. Mouthparts rufo-testaceous, similar to other appendages toward apices. Pronotum with lateral margin elevated, sinuate, hind angle acute; basal impression smooth. Elytron iridescent purple-pink; intervals flat, interneurs shallowly striatiopunctate. 125. Platynus B. 9.60 mm, 1400 m, D., Macropterous. 253 Body black. Scape black, but remaining antennomeres lighten apically to rufo- testaceous. Pronotum sinuate, elevated along length of margin, hind angle rectangular. Elytra with sides parallel, all interneurs punctate. Legs black except tarsi rufo-testaceous. XVI. Pterosticini 126. Abarys A. 5.56 mm, 750 m, P., Macropterous. Body brassy and shiny. Eyes large. Head appendages rufo-testaceous. Pronotum as wide basally as elytra, sinuate, basal impressions short and linear. Legs rufous. 127. Blennidus A. 12.95 mm, 2000 m, Macropterous. Mentum with blunt/truncated tooth. Mandibles scythe-like. Plica not crossed like most Pterostichini. 128. Blennidus B. 12.28 mm, 1750 m, D., Micropterous. Body black. Antennae lighter. Pronotum longer than wide and effaced with linear basal impressions and quadrate hind angle. Elytra robust, deep interneurs and elevated intervals. Tarsi light, front femora somewhat dilated. 129. Loxandrus A. 8.47 mm, 1400 m, D., Macropterous. Body black. Antenna testaceous, darker basally; palp testaceous. Pronotum wider at apex than base, hind angle acute; basal impression linear. Elytron with deep interneurs. Legs infuscate, tarsus testaceous. 130. Loxandrus B. 8.99 mm, 1400 m – 2000 m, D., Macropterous. Pronotum wide, hind angle acute; lateral margin slightly lighter. Metasternum long. Elytron with rainbow iridescence. White spot in apical 1/3 elytra towards suture. Appendages rufo-testaceous. 254 131. Loxandrus C. 6.46 mm, 500 m, P., Macropterous. Similar to Loxandrus B, but with two elytral spots (one apical, one basal), basal spot is sutural. All appendages flavous. 132. Loxandrus D. 8.06 mm, 500 m, P., Macropterous. Appendages flavous. Pronotum round. Elytra with rainbow iridescence, punctate. Similar to Loxandrus B and Loxandrus C but with no elytral spots. 133. Pseudobarys A. 11.40 mm, 2000 m, D., Brachypterous-D. Body rufous. Mandibles long. Antenna, palp light. Pronotum with apical and hind angle acute, sharp. Elytron dull matte. 134. Stolonis A. 7.83 mm, 800 m, D., Macropterous. Body black. Appendages flavous, Antennae multicolored: 1-3 flavous, apical 2/3 of 4 -7 black, 8 – 10 white-flavous, 11 brown-black. Pronotum cordate, base approx.. 1/2 width of middle, base quadrate but rounded and punctate. Elytra with rainbow iridescence 135. Stolonis B. 5.56 mm, 1400 m, D., Micropterous. Antennomeres pale yellow except 4-7 and 11 darker. Palps pale yellow. Pronotum large, widest at apical 1/3, basal impressions short linear, basal margin punctate. Elytra with interneurs punctate. Pronotal and elytral lateral margins (and elytral sutural margins) translucent. Legs pale yellow. 136. Trichonilla A. 16.44 mm, 1400 m, D., Micropterous. Body markedly black. Palp paler, palpomere 4 triangular. Antenna paler from antennomere 6 to apex. Pronotum with lateral margin sinuate, lateral bead complete; basal impression deep, linear. Legs black. 255 XVII. Scaritini 137. Glyptogrus A. 23.41 mm, 2000 m, O.G., Micropterous. Color similar to Scarites A. Elytra with interneurs 2 and 4 with carinae/costae through entire length of elytra, remaining interneurs essentially obsolete. 138. Scarites A. 23.64, 3650 m, O.G., Micropterous. Body black. Mandibles large. Head appendages rufous. Pronotum quadrate, hind angle obsolete. Elytral humerus with lateral carinae, interneurs somewhat shallow. XVIII. Trechini 139. Oxytrechus A. 2.76 mm, 2500 m ‒ 3250 m, O.G., Micropterous. Pronotum cordate, hind angle almost obsolete. but looks obtuse around hind setae. Elytra effaced with rainbow iridescence, interneurs absent. 140. Oxytrechus B. 2.86 mm, 2750 m, O.G., Micropterous. Similar to Oxytrechus A but hind angle slightly denticulate. Appendages flavous. 141. Paratrechus A. 4.97 mm, 3000 m – 3250 m, D., O.G., Micropterous. Body red-brown, sulcus on head darker. Antennae and palps flavous. Pronotum with lateral margin translucent, flattened and slightly widens toward base where it is elevated slightly, hind angle acute. Elytra round, slight iridescent shimmer, shallow interneurs. Legs slightly lighter than body. 142. Paratrechus B. 5.41 mm, 3250 m, O.G., Micropterous. Brown body. Long mandibles. Pronotum quadrate, basal impressions circular and deep, hind angle rectangular-acute. Elytral interneurs slightly shallowly punctate, slight rainbow iridescence. Elytra fused. 143. Paratrechus C. 4.74 mm, 2500 ‒ 3650 m, D., O.G., Micropterous. 256 Body infuscate. All appendages testaceous (except femur only). Pronotum cordate with lateral margin translucent and elevated, especially basally, hind angle almost rectangular, widest part is as wide as base of elytra. Elytron with apical costa at interval 8, shallowly punctate elytra, rounded, not parallel, wider than pronotum. Elytron fused. 144. Trechischibus A. 5.08 mm, 2500 m ‒ 3400 m, D., O.G., Dimorphic-GH. Very narrow, parallel body. Mandibles long. All appendages testaceous, but femur infuscate. Pronotum with hind angle obtuse with slight denticulation, at widest part less wide than base of elytra. Elytron with rainbow iridescence, interneurs shallow, nearly effaced, margins translucent. Elytra fused. Variable species. 145. Trechischibus B. (4.99 mm, 3250 m ‒ 3400 m, O.G., Micropterous. Body red-brown. Sulcus on head darker. palps and antennae flavous. Pronotum with lateral margin translucent, widens toward base where it is slightly elevated, hind angle acute. Elytra with apical costae at interval 8. Elytra very round, slight iridescent shimmer, and glabrous, interneurs obsolete, apex like a point. Elytra fused. Legs slightly lighter than body. (aka T. obesus) 146. Trechischibus C. 5.43 mm, 3250 m ‒ 3400 m, O.G., Micropterous. Similar to Trechischibus A. Pronotum narrows basally, less wide than base of elytra, hind angle with very small tooth. Ventral sterna dark. 147. Trechischibus D. 5.01 mm, 3000 m – 3400 m, O.G., Micropterous. Body dark. Appendages testaceous. Pronotum also narrows basally. Elytral interneurs shallow. 257 148. Trechischibus E. 4.61 mm, 2500 m, D., O.G., Micropterous. Body black. Head appendages flavous. Pronotum with lateral margins translucent and wide, hind angle obtuse and smooth. Elytra with rainbow iridescence, interneurs almost obsolete. Legs dark, lighter apically 149. Trechischibus F. 3.96 mm, 3450 m ‒ 3650 m, D., OG Micropterous. Body dark. Head appendages flavous. Pronotum with lateral margin sinuate, margin translucent, basal impressions deep, round. Elytral margin translucent. Legs flavous except for femora. 150. Trechischibus G. 4.63 mm, 3000 m, O.G., Micropterous. Pronotum almost sinuate, lateral margin widens toward base with acute angle. Legs flavous. Both specimens teneral. 151. Trechischibus H. 5.03 mm, 3250 m, O.G., Micropterous. Similar to Trechischibus F but larger. Body red-brown. Pronotum somewhat sinuate, hind angle rectangular, basal impressions deep and broad across base. 152. Trechischibus I. 4.35 mm, 2250 m – 2500 m, D., O.G., Micropterous. Body dark. Pronotum with margin flattened (widens at base), basal impression obsolete, hind angle rectangular and distinct. Legs flavous, femora darker. 153. Trechischibus J. 5.29 mm, 2500 m ‒ 3400 m, D., O.G., Micropterous. Body red. Head appendages orange-flavous. Body uniformly wide, pronotum almost as wide as elytra at base. Pronotum with margin like Trechischibus I, but flattened margin continues basally. Elytral interneurs shallow. Legs same color as body. XIX. Zuphiini 258 154. Pseudaptinus A. 6.14 mm, 3000 m, D., Micropterous. Body rufous, appendages lighter. Body shape similar to Formicidae (head shape, “waist,” etc.). Eyes small. Body entirely setose. Pronotum cordate with lateral margin sinuate, hind angle obtuse. Elytral humeri narrow. 259 Figure A1. Illustrations of elytral markings on select carabid beetle species (by S.A.Maveety). Mean standard body length (SBL) 3 (length of elytra, dorsal) is listed with each morphospecies. A) Bembidion Q, B) Bembidion R, C) Pseudophorticus E, D) Apenes A, E) Apenes C, F) Lebia C, G) Lebia D. 260 CURRICULUM VITAE SARAH A. MAVEETY Department of Biology, Wake Forest University Winston-Salem, NC, 27106 phone: (336) 758-4731 [email protected] EDUCATION Ph.D., Candidate, Biology, Wake Forest University, Winston-Salem, NC Dissertation: Ecology of ground dwelling carabid beetles (Coleoptera: Carabidae) in the Peruvian Andes. Advisor: Dr. Robert A. Browne Expected December 2013 B.S. in Biology, Wake Forest University, Winston-Salem, NC Graduated, Cum Laude, May 2007 PROFESSIONAL EXPERIENCE Teaching Assistant, August 2008 – May 2013 Wake Forest University, Winston-Salem, NC . Genetics and Molecular Biology (BIO 213) Fall 2011 – Spring 2013 . Ecology and Evolution, (BIO 113) Fall 2009 – Spring 2011 . Biological Principles, (BIO 111) Spring 2009 . Biology and the Human Condition (BIO 101), Fall 2008 Research Assistant, May 2005 – May 2007 Wake Forest University, Winston-Salem, NC Dr. Robert A. Browne, Advisor, Department of Biology “Community Composition of Carabids (Coleoptera) in the Spruce-Fir Sky Islands of the Southern Appalachian Mountains” OTHER ACADEMIC EXPERIENCE/SKILLS Software Skills: Microsoft Excel, Microsoft Word, Microsoft PowerPoint, ESRI ArcGIS (Spatial, 3-D, Network Analyst), Idrisi, Garmin, Garmin DNR Statistical Software Skills (R, EstimateS) Experience: Basic GIS tools, Image processing, remote sensing products, cartographic models, map design and layout, field data collection, geo-registration, project work, group projects, time management 261 CERTIFICATION College Reading and Learning Association Certification, Wake Forest University Learning Assistance Center, Spring 2006 PUBLICATIONS Maveety S.A., R.A. Browne, & T.L. Erwin (2011) Carabidae diversity along an altitudinal gradient in a Peruvian cloud forest (Coleoptera). Zookeys 147:651-666. Maveety S.A., R.A. Browne, & T.L. Erwin. Carabid beetle diversity related to altitude and seasonality in the Peruvian Andes. Studies on Neotropical Fauna and Environment Submitted April 2013. Browne R.A., S.A. Maveety, E.L. Cooper, K.N. Riley. Ground beetle (Coleoptera: Carabidae) species composition in the southern Appalachian Mountains. Southeastern Naturalist Submitted August 2013. Maveety S.A., R.A. Browne. Patterns of carabid beetle (Coleoptera: Carabidae) morphology along an altitudinal gradient. Ecological Entomology Submitted August 2013. Maveety S.A., R.A. Browne. Effect of disturbance and interannual variation on carabid beetle assemblages in a Peruvian montane cloud forest. In prep: Journal of Tropical Ecology. Maveety S.A., R.A. Browne. Carabid beetle assemblages (Coleoptera: Carabidae) on Andes and Appalachian cloud forest gradients. In prep: Environmental Entomology. PRESENTATIONS Maveety, S.A. Carabid beetle diversity along a Peruvian altitudinal gradient. Department of Biology Seminar Series, Wake Forest University. Winston-Salem, NC. 24 April 2013. Maveety S.A., R.A. Browne. Body size and dispersal ability of carabid beetles (Coleoptera: Carabidae) on an elevation gradient in a Neotropical cloud forest. Paper Presentation. Entomological Society of America Annual Meeting. Knoxville, TN. 12 November 2012. Maveety S.A., R.A. Browne. Carabid beetles on an altitudinal gradient: spatial and temporal diversity. Paper Presentation. Entomological Society of America Annual Meeting. San Diego, CA. 13 December 2010. *President’s Prize Recipient Maveety S.A. Research synopsis for Systematics, Evolution, and Biodiversity Branch Meeting at the Entomological Society of America’s Annual Meeting, invited. San Diego, CA. 13 December 2010. Maveety S.A., R.A. Browne. Ground beetle (Coleoptera: Carabidae) diversity as related to altitude in tropical montane cloud forests of Perú. Paper Presentation. Ecological Society of America Annual Meeting. Pittsburg, PA. 5 August 2010. 262 Maveety S.A., R.A. Browne. Ground beetle (Coleoptera: Carabidae) diversity as related to elevation in Peruvian cloud forests. Poster Presentation. Association for Southeastern Biologists Annual Meeting, Asheville, NC. April 9, 2010. Maveety S.A., R.A. Browne. Patterns of Carabid (Coleoptera) diversity along Nearctic and Neotropical altitudinal gradients. Poster Presentation. Entomological Society of America, Southeastern Branch Annual Meeting. Atlanta, GA. 8 March 2010. Maveety, S.A. Ground beetle (Coleoptera: Carabidae) diversity as related to elevation in Peruvian cloud forests. Department of Biology Seminar Series, Wake Forest University. Winston-Salem, NC. 18 November 2009. AWARDS/HONORS Species name dedication, Andinodontis maveetyae (Coleoptera: Carabidae); [IN: Erwin TL, L Toledano, & DR Maddison (2010) New enigmatic species of ground beetles from stream margins and scree in the Andes of South America (Carabidae, Trechitae, Andinodontis n. gen.). Ent. Bl. 106:73:88.] Research Student, National Museum of Natural History, Smithsonian Institution, Feb 2009 to Jan 2012 and Feb 2012 to Jan 2015 Vecellio Grant, Wake Forest University Department of Biology, Summer 2008 and Springs 2009, 2010, & 2011 Elton C. Cocke Travel Award, Wake Forest University Dept. of Biology, Dec 2010 and Nov 2012 Graduate School Alumni Travel Fund , August 2010 and November 2012 Entomological Society of America Systematics Evolution and Biodiversity Section – Student Travel Award Recipient, Summer 2010 Tuttle-Newhall Fund, Wake Forest University Dept. of Biology, Dec 2009 NSF Graduate Research Fellowship Honorable Mention, 2009-2010 Application Fulbright Scholar, 2007-2008, Peru EDUCATIONAL TRAVEL Costa Rica, International Studies Abroad, Fall 2005 Universidad Latinoamericana de Ciencia y Tecnología, San José “Marine Biology” and “Tropical Ecology” Peru, Wake Forest University, Summer 2005 Instructor, Dr. Miles R. Silman “Tropical Biodiversity” 263 PROFESSIONAL AFFILIATIONS / MEMBERSHIPS Graduate Student Association, Wake Forest University Biology Department Student Representative, August 2010 – May 2012 Reynolda Campus Co-Chair to the Executive Committee, Feb 2012 – present Association for Southeastern Biologists (ASB), 2009 – Present Association for Tropical Biology and Conservation (ATBC), 2009 - Present Ecological Society of America (ESA), 2009 - Present Entomological Society of America (ESA), 2008 – Present COMMUNITY INVOLVEMENT/ VOLUNTEER WORK YMCA Literacy Initiative ESL tutoring, Fall 2009 to Fall 2010 Central YMCA, Winston-Salem, NC Science Olympiads Volunteer Coach, Fall 2006 – Spring 2007, Paisley Middle School, Winston-Salem, NC Volunteer Judge, March 10, 2012, Atkins Academic and Technology High School, Winston-Salem, NC FOREIGN LANGUAGE ABILITIES Spanish – Reading, writing, spoken fluency 264